INTERNATIONAL SERIES OF MONOGRAPHS ON
PURE AND APPLIED BIOLOGY
Division: ZOOLOGY
General Editor: G. A. Kerkut
Volume 4
IMPLICATIONS OF EVOLUTION
OTHER TITLES IN THE SERIES ON PURE AND
APPLIED BIOLOGY
Zoology Division
Vol. 1. RAVEN — An Outline of Developmental Physiology.
Vol. 2. RAVEN — Morphogenesis: The Analysis of Molluscan
Development .
Vol. 3. SAVORY— Instinctive Living.
Biochemistry Division
Vol. 1. The Thyroid Hormones.
Botany Division
Vol. 1. BOR — Grasses of India, Burma and Ceylon.
Vol. 2. TURRILL— Vistas in Botany.
Vol. 3. SCHULTES— Orchids of Trinidad and Tobago.
Modern Trends in Physiological Sciences Division
Vol. 1. FLORKIN — Unity and Diversity in Biochemistry.
Vol. 2. BRACHET — The Biochemistry of Development.
Vol. 3. GEREBTZOFF— Cholinesterases.
Vol. 4. BROUHA — Physiology in Industry.
K '/£
IMPLICATIONS OF
EVOLUTION
By
G. A. KERKUT
M.A., PH.D.
Department of Physiology and Biochemistry
The University of Southampton
PERGAMON PRESS
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1960
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iNTS
Preface vii
Acknowledgements ix
1 INTRODUCTION 1
2 BASIC ASSUMPTIONS 6
3 VIRUSES, RICKETTSIAE AND BACTERIA 18
4 THE PROTOZOA 26
5 ORIGIN OF THE METAZOA 36
6 THE MOST PRIMITIVE METAZOA 50
(1) PORIFERA 54
(2) MESOZOA 71
(3) COELENTERATA 76
(4) CTENOPHORA 84
(5) PLATYHELMINTHES 94
7 THE INVERTEBRATE PHYLA 101
8 BIOCHEMICAL STUDIES OF PHYLOGENY 112
(1) PHOSPHAGENS 112
(2) STEROLS 129
9 VERTEBRATE PALAEONTOLOGY 134
10 CONCLUSIONS 150
vi CONTENTS
Page
Bibliography 159
Name Index 169
Subject Index 171
PREFACE
There are many books about Evolution so perhaps in this preface
I should state what this book is not about. It is not concerned with
the mechanism of speciation, the evolution of dominance, the
relationship of enzymatic adaptation to the inheritance of acquired
characteristics or the probability that Natural Selection can bring
about a pandemic of rodents in n + 1 years. Instead the present
book is concerned with an examination of certain basic assumptions
and implications that have become involved in the present-day
concept of the evolutionary relationships within the animal
kingdom. The majority of books on Evolution either blatantly
treat these assumptions as part of an old (and concluded) historic
argument or else they avoid discussing the assumptions and
instead deal with the more scientific and mathematical parts of
Evolution.
If one tries to question this avoiding reaction, the protagonists
round on one and say in an accusing tone of voice, " Don't you
believe in the Theory of Organic Evolution? What better theory
have you got to offer? "
May I here humbly state as part of my biological credo that I
believe that the theory of Evolution as presented by orthodox
evolutionists is in many ways a satisfying explanation of some of
the evidence. At the same time I think that the attempt to explain
all living forms in terms of an evolution from a unique source,
though a brave and valid attempt, is one that is premature and
not satisfactorily supported by present-day evidence. It may in
fact be shown ultimately to be the correct explanation, but the
supporting evidence remains to be discovered. We can, if we like,
believe that such an evolutionary system has taken place, but I
for one do not think that " it has been proven beyond all reason-
able doubt." In the pages of the book that follow I shall present
evidence for the point of view that there are many discrete groups
vii
viii PREFACE
of animals and that we do not know how they have evolved nor
how they are interrelated. It is possible that they might have
evolved quite independently from discrete and separate sources.
There are only a limited number of chemical elements that are
capable of forming stable polymerisation compounds and it is not
at all surprising that the same compounds have been formed on
several occasions. Quite complex materials such as carbohydrates,
peptides and even nucleic acids can be formed by irradiating water
containing simple salts and gases.
It may be suggested that the problem we are examining here,
namely that of the evolution and interrelationship of the basic
living stocks is a major problem and one that will test the strength
and ability of many hundreds of research workers. If this book
merely indicates to some of the readers that certain lines of thought
are still open to examination, then I shall consider that it has done
its allotted task.
There is, however, a second point that I should like to make, and
this concerns not factual material but an attitude of mind. It is
very depressing to find that many subjects are becoming encased
in scientific dogmatism. The basic information is frequently over-
looked or ignored and opinions become repeated so often and so
loudly that they take on the tone of Laws. Although it does take a
considerable amount of time, it is essential that the basic informa-
tion is frequently re-examined and the conclusions analysed.
From time to time one must stop and attempt to think things out
for oneself instead of just accepting the most widely quoted
viewpoint. I have dealt with this attitude in the introductory
chapter of this book, though I hope that the moral does not end
there but instead runs through the rest of the book as well.
It is a pleasure to acknowledge the kind help and assistance
that various colleagues have given me during the writing of this
work. Many of them have read through parts of the book or
offered advice on various points. I have profited greatly from their
counsel, though of course I bear full responsibility for all the
statements and errors. In particular I should like to thank
Professor E. Baldwin, Drs. M. S. Laverack, K. A. Munday,
S. Smith, Miss D. Wisden, Messrs. Robert Walker, Edward
Munn, and Richard Solly for their help and forbearance.
ACKNOWLEDGEMENTS
I am grateful to the following authors and publishers for
permission to use figures and to quote from their publications:
Professor G. Schramm for kindly providing the photograph
from which Fig. 2 was taken.
Dr. S. Brenner and Dr. R. W. Home for kindly providing the
photograph from which Fig. 3 was taken.
Academic Press for permission to quote from the article by
H. A. Krebs in Chemical Pathways in Metabolism. Vol. 1, edited
by D. M. Greenberg.
Allen and Unwin for permission to quote from the article by
G. R. de Beer in " The evolution of the Metazoa " from the book
Evolution as a Process edited by J. Huxley, A. C. Hardy and E. B.
Ford.
Cambridge University Press for permission to take the table
printed on page 112 from Comparative Biochemistry by E. Baldwin;
the table on page 2 from The Cambridge University Handbook;
and the quotations from Biochemistry and Morphogenesis by J.
Needham, and Growth and Form by W. D'Arcy Thompson.
Masson et Cie for permission to reproduce Figs. 7, 8, 9, 11, 12, 15,
and 16, from Traite de Zoologie edited by P. P. Grasse.
McGraw Hill for permission to reproduce Figs. 25 and 27,
taken from The Invertebrates by L. H. Hyman, and also for
permission to quote from this work.
Oxford University Press for permission to quote from E. Radl's
History of Biological Theories and to adapt Fig. 43 from The Horses
by G. G. Simpson.
Charles C. Thomas for permission to quote from a paper by
H. A. Krebs published in the Harvey Lectures.
John Wiley for permission to take the table on page 20 from
General Biochemistry by J. S. Fruton and S. Simmons.
IX
X ACKNOWLEDGEMENTS
I should also like to thank the editors of the following journals
for permission to copy and reproduce material. Archive de Zoo-
logie General et Experimentale ; Biochemistry, Biophysics Acta;
Biochemical Journal; Journal of Bacteriology; Journal of Experi-
mental Biology; Proceedings of the Royal Society; Quarterly Review
of Biology ; Systematic Zoology and Zoologiska Bidrag.
'
1 t
>
CHAPTER 1
INTRODUCTION
Throughout the Dark and Middle Ages, Learning was under the
aegis of the Church. Except for useful subjects such as Medicine
and perhaps Law, the university students were concerned with
material that would either make the student a useful priest or else
a person useful to priests.
The hold that the Church has had on the universities has been
but slowly relinquished over the years. Until 1871 it was the custom
for the majority of dons at Cambridge to be ordained before they
could carry out any of the duties in college. This did not always
mean that the prospective Fellow had to make a careful study of
theology. Thus the Fellows of some colleges had the right of be-
coming ordained in their own chapel as soon as they were elected to
a Fellowship without having to undergo any arduous extra study.
This special sanction was taken away from them in 1852 and from
then on they had to become ordained in the normal manner.
The Fellows besides being compulsorily ordained also had to
live under an enforced celibacy. Should they wish to enjoy the
varied pleasures of married life they had in turn to relinquish
their college Fellowships. The married clergyman then left
Cambridge and usually took up one of the livings that were in the
gift of his college. This had its own compensations ; those scholars
who had swallowed their intellectual goat in their youth, instead
of being forced to eke it out to various undergraduates for the rest
of their lives, could leave Cambridge and take up a rich living in
the outside world. This made more room available at the university
for the younger man, who did not then merely have to wait for
his older colleagues to die.
The hold of the Church on the university continued in many
ways. The undergraduates coming up to Cambridge until 1852
1
2 INTRODUCTION
had to be communicants of the Church of England, and the
undergraduate coming up in, say, 1910 had to satisfy his examiners
not only in his knowledge of classical languages but also had to
show that he had some knowledge of Archdeacon William Paley's
book on Evidences of Christianity. The latter examination was in
force till 1927, when it was brought to the notice of the university
authorities that many undergraduates did not in fact read Paley's
Evidences but instead studied a little crib of them. Many of the
more sceptical dons in the university were in favour of retaining
the examination and ensuring that all undergraduates should
be made to study Paley's Evidences most carefully, " For in this
way," they said, " the student will be forced to realise just how
weak the evidence in favour of Christianity really is." This
argument was not upheld and in 1927 another piece of tradition was
abandoned.
Many present-day undergraduates seem to imagine that the
various subjects they study have existed as such, if not for
eternity, then at least from time immemorial. They are surprised
to learn that many of the chairs and examinations only came into
existence over the last half-century. In the table below I have
selected a few of the dates at which various chairs became
established at Cambridge. It will be seen that the subjects of
Theology and Medicine are very ancient whilst German, French
and English are relatively modern.
Establishment of Chairs at Cambridge
1502 2 Chairs of Divinity
1540 Civil Law, Physic, Hebrew, Greek
1634 Arabic
1683 Moral Philosophy
1684 Philosophy
1702 Organic Chemistry
1704 Astronomy
1707 Anatomy
1724 History
1727 Botany
1866 Zoology
1869 Fine Art
1909 German
INTRODUCTION 3
1911 English Literature
1919 French
1937 Geography
1938 Education
(This is only a selection from the complete list.)
You may ask, " What has all this got to do with evolution? "
It is my thesis that many of the Church's worst features are still
left embedded in present-day studies. Thus the serious under-
graduate of the previous centuries was brought up on a theological
diet from which he would learn to have faith and to quote authori-
ties when he was in doubt. Intelligent understanding was the
last thing required. The undergraduate of today is just as bad;
he is still the same opinion-swallowing grub. He will gladly
devour opinions and views that he does not properly understand
in the hope that he may later regurgitate them during one of his
examinations. Regardless of his subject, be it Engineering,
Physics, English or Biology, he will have faith in theories that he
only dimly follows and will call upon various authorities to
support what he does not understand. In this he differs not one
bit from the irrational theology student of the bygone age who
would mumble his dogma and hurry through his studies in order
to reach the peace and plenty of the comfortable living in the world
outside. But what is worse, the present-day student claims to be
different from his predecessor in that he thinks scientifically and
despises dogma, and when challenged he says in defence, "After
all, one has to accept something, or else it takes a very long time to
get anywhere."
Well, let us see the present-day student " getting somewhere."
For some years now I have tutored undergraduates on various
aspects of Biology. It is quite common during the course of
conversation to ask the student if he knows the evidence for
Evolution. This usually evokes a faintly superior smile at the
simplicity of the question, since it is an old war-horse set in count-
less examinations. " Well, sir, there is the evidence from
palaeontology, comparative anatomy, embryology, systematics and
geographical distributions," the student will say in a nursery-
rhyme jargon, sometimes even ticking off the wrords on his fingers.
He would then sit and look fairly complacent and wait for a more
2— IOE
4 INTRODUCTION
difficult question to follow, such as the nature of the evidence for
Natural Selection. Instead I would continue on with Evolution.
" Do you think that the Evolutionary Theory is the best
explanation yet advanced to explain animal interrelationships? "
I would ask.
1 Why, of course, sir," would be the reply in some amazement
at my question. " There is nothing else, except for the religious
explanation held by some Fundamentalist Christians, and I
gather, sir, that these views are no longer held by the more
up-to-date Churchmen."
" So," I would continue, " you believe in Evolution because
there is no other theory? "
" Oh, no, sir," would be the reply, " I believe in it because of
the evidence I just mentioned."
" Have you read any book on the evidence for Evolution? "
I would ask.
" Yes, sir," and here he would mention the names of authors
of a popular school textbook, " and of course, sir, there is that
book by Darwin, The Origin of Species."
" Have you read this book? " I asked.
" Well, not all through, sir."
" About how much? "
" The first part, sir."
" The first fifty pages? "
" Yes, sir, about that much; maybe a bit less."
" I see, and that has given you your firm understanding of
Evolution? "
" Yes, sir."
" Well, now, if you really understand an argument you will
be able to indicate to me not only the points in favour of the
argument but also the most telling points against it."
I suppose so, sir."
Good. Please tell me, then, some of the evidence against the
theory of Evolution."
Against what, sir? "
The theory of Evolution."
" But there isn't any, sir."
Here the conversation would take on a more strained atmosphere.
The student would look at me as if I was playing a very unfair
a
a
INTRODUCTION 5
game. It would be clearly quite against the rules to ask for
evidence against a theory when he had learnt up everything in
favour of the theory. He also would take it rather badly when I
suggest that he is not being very scientific in his outlook if he
swallows the latest scientific dogma and, when questioned, just
repeats parrot fashion the views of the current Archbishop of
Evolution. In fact he would be behaving like certain of those
religious students he affects to despise. He would be taking on
faith what he could not intellectually understand and when
questioned would appeal to authority, the authority of a " good
book " which in this case was The Origin of Species. (It is inter-
esting to note that many of these widely quoted books are read
by title only. Three of such that come to mind are the Bible, The
Origin of Species and Das Kapital.)
I would then suggest that the student should go away and read
the evidence for and against Evolution and present it as an essay.
A week would pass and the same student would appear armed with
an essay on the evidence for Evolution. The essay would usually
be well done, since the student might have realised that I should
be tough to convince. When the essay had been read and the
question concerning the evidence against Evolution came up, the
student would give a rather pained smile. " Well, sir, I looked up
various books but could not find anything in the scientific books
against Evolution. I did not think you would want a religious
argument." " No, you were quite correct. I want a scientific
argument against Evolution." " Well, sir, there does not seem to
be one and that in itself is a piece of evidence in favour of the
Evolutionary Theory."
At this piece of logic the student would sit back and feel that
he had come out on top. After all, I had merely been questioning
him whilst he had produced information.
I would then indicate to him that the theory of Evolution was
of considerable antiquity and would mention that he might have
looked at the book by Radl, The History of Biological Theories.
Having made sure that the student had noted the book down for
future reference I would proceed as follows.
'
CHAPTER 2
BASIC ASSUMPTIONS
Before one can decide that the theory of Evolution is the best
explanation of the present-day range of forms of living material
one should examine all the implications that such a theory may
hold. Too often the theory is applied to, say, the development of
the horse and then because it is held to be applicable there it is
extended to the rest of the animal kingdom with little or no further
evidence.
There are, however, seven basic assumptions that are often
not mentioned during discussions of Evolution. Many evolution-
ists ignore the first six assumptions and only consider the seventh.
These are as follows.
(1) The first assumption is that non-living things gave rise to
living material, i.e. spontaneous generation occurred.
(2) The second assumption is that spontaneous generation
occurred only once.
The other assumptions all follow from the second one.
(3) The third assumption is that viruses, bacteria, plants and
animals are all interrelated.
(4) The fourth assumption is that the Protozoa gave rise to the
Metazoa.
(5) The fifth assumption is that the various invertebrate phyla
are interrelated.
(6) The sixth assumption is that the invertebrates gave rise to
the vertebrates.
(7) The seventh assumption is that within the vertebrates the
fish gave rise to the amphibia, the amphibia to the reptiles, and
the reptiles to the birds and mammals. Sometimes this is expressed
in other words, i.e. that the modern amphibia and reptiles had a
common ancestral stock, and so on.
6
BASIC ASSUMPTIONS 7
For the initial purposes of this discussion on Evolution I shall
consider that the supporters of the theory of Evolution hold that
all these seven assumptions are valid, and that these assumptions
form the " General Theory of Evolution."
The first point that I should like to make is that these seven
assumptions by their nature are not capable of experimental
verification. They assume that a certain series of events has
occurred in the past. Thus though it may be possible to mimic
some of these events under present-day conditions, this does not
mean that these events must therefore have taken place in the
past. All that it shows is that it is possible for such a change to
take place. Thus to change a present-day reptile into a mammal,
though of great interest, would not show the way in which the
mammals did arise. Unfortunately we cannot bring about even
this change; instead we have to depend upon limited circum-
stantial evidence for our assumptions, and it is now my intention
to discuss the nature of this evidence.
Non-living into living (Biogenesis)
This is one of the oldest problems to puzzle man. Is it possible
for non-living material simply to be turned into living material
or is some extra " vital " force necessarv? It is reasonablv clear
that living bodies in many ways use systems similar to those
present in the non-living world. One of the first barricades
appeared to fall to Wohler, when he showed by his synthesis of
urea that there was no very clear distinction between organic
chemicals and non-organic chemicals. Within recent years we
have been able to devise systems in wThich the irradiation of a
mixture containing water, carbon dioxide and ammonia brings
about the formation of amino-acids, simple peptides, and
carbohydrates. However, proteins and nucleoproteins have not
yet been synthesised under such conditions and these latter com-
pounds appear to be of great importance in the development and
maintenance of life. One imagines that the synthesis of these
substances will merely be a matter of time and application, but
it will be useful to distinguish the two different methods of
achieving their synthesis. The first is to try to synthesise them
under conditions in which we imagine that living things first
occurred, i.e. to irradiate simple solutions and hope that proteins
8 BASIC ASSUMPTIONS
and nucleoproteins will form by random combination. This
would mimic the conditions under which we believe life originated.
The second method is to use specialised chemical and physical
techniques to synthesise proteins and nucleoproteins, and having
synthesised them, then to place them in their correct structural
relationship. In this way, the combination of synthetic proteins,
nucleic acids, lipids and carbohydrates might lead to the forma-
tion of a simple virus-like compound that could reproduce in
living cells. The next stage would be the development of an
artificial solution to maintain the artificial virus. With these steps
accomplished we should have learnt a great deal about the processes
taking place in the living body and no doubt we should have dis-
covered new rules for physics and chemistry, but we could not
say from our experiments that the living material in the universe
arose in this way. The results would show that living matter can
arise by synthetic methods devised in the laboratory, but it
would still be possible that there were other methods by which life
actually arose in the universe. For a full discussion of the origin
of life one should consult the following articles: Oparin (1957);
Bernal (1954); Pringle (1954); Pirie (1954); Haldane (1954).
Life arose only once
The assumption that life arose only once and that therefore *
all living things are interrelated is a useful assumption in that it
provides a simple working basis for experimental procedure. But
because a concept is useful it does not mean that it is necessarily
correct. The experimental basis for this concept in particular is
not as definite and as conclusive as many modern texts would have
us believe.
Biochemical evidence. Biochemists and comparative physi-
ologists usually assume that all protoplasm, no matter where it is
found, has the same fundamental biochemical and biophysical
processes taking place in it. But even an elementary study of the
situation shows that there are often many different ways of
carrying out a simple process in the animal kingdom. One well-
known example is that of carrying oxygen in solution; various
substances such as haemoglobin, haemocyanin, haemerythrin and
chlorocruorin are known to be capable of combining with oxygen.
But the common possession of a specific blood pigment does not
BASIC ASSUMPTIONS 9
indicate any close phylogenetic relationship. Thus though many
Crustacea have haemocyanin no biochemist or physiologist would
suggest taking Daphnia out of the Crustacea because it possesses
haemoglobin. The role of blood pigments has been much studied
and in particular we accept the varied way in which they are dis-
tributed throughout the animal kingdom. Even here we do not
always know their function ; thus we find haemoglobin in the root
nodules of leguminous plants (Keilin and Wang 1945), where its
precise function is as yet not known. Plants, however, seem
capable of synthesising many substances that are often regarded
as " mammalian " compounds. Nettle stings contain acetyl
choline, 5-hydroxytryptamine and histamine, and it is probable
that these have been independently developed by the higher
plants.
There are in the world but some ninety elements, and of these
only a few such as carbon, nitrogen, oxygen, hydrogen, phosphorus
and sulphur appear capable of forming natural monomers and
polymers. It is therefore not surprising that these elements are
united to form compounds such as citric acid or 5-hydroxy-
tryptamine in widely separated plants and animals. Such a
synthesis might have occurred independently on many occasions
by trial and error. It should be remembered that there is no
Patent Law in the natural world, and though one can simplify
the situation by use of William of Occam's razor, the careless
use of such a weapon can at times be suicidal.
Our ignorance is even greater in other biochemical fields, yet it
is often stated that all protoplasm shows the same fundamental
biochemical systems. The most quoted example is the way in
which protoplasm oxidises carbohydrates to liberate energy. This
release of energy is obtained through two biochemical cycles,
the glycolysis cycle (Embden-Meyerhof) and the tricarboxylic
acid cycle (Krebs). Many of the chemicals present in these two
cycles have been found in bacteria, protozoa, plants, lower
metazoa, birds and mammals, and because some of the ingredients
are present it is assumed that the whole system is present. The
argument then runs that because the system is very complex, it
would be too much to expect that each group developed this
complex system independently and so protoplasm everywhere
must have had a common origin.
10 BASIC ASSUMPTIONS
Krebs in 1948 discussed the universality of the tricarboxylic
cycle in cells and tissues. He stated, " there is no doubt that yeast
cells can synthesise succinate in the presence of glucose, and
citrate in the presence of acetate, but none of the strains of
baker's and brewer's yeast tested at the Sheffield laboratory was
found capable of oxidising succinic or citric acids at a significant
rate under whatever conditions these substances were tested."
In 1954 he was of much the same opinion: " thus all the enzyme
systems required for the tricarboxylic cycle are present in yeast
cells and there can be no doubt that the cycle can take place. . . .
However, these findings are not decisive evidence for the assump-
tion that the cycle is the main terminal respiratory process in
yeasts. ... In many other organisms another terminal oxidation
mechanism seems to play a major role. Its nature is unknown in
the case of yeast. It may be a dicarboxylic acid cycle in certain
bacteria." It now appears that the events that suggested the
existence of a dicarboxylic acid cycle in bacteria may be better
explained in terms of a divergence from the tricarboxylic acid
cycle (Romberg 1958). The system of terminal oxidation in
yeasts is still obscure.
In effect, then, the situation in bacteria, yeasts, plants and the
lower animals is not as simple or clear cut as might be imagined.
There is more than one pathway for the breakdown of carbo-
hvdrates, and the glycolysis cycle and the citric acid cycle are but
two of many that are in the process of elucidation. Thus recently
a hexose monophosphate shunt has been described as an alterna-
tive method by which bacteria and many animal tissues break down
glucose. This, combined with the possibility of an alternative
terminal oxidation system, enables us to postulate two more
systems that may be active in tissue metabolism. This view is
supported by Cohen (1955a), who in his account of alternative
pathways in carbohydrate metabolism states, " the time is past
when we uncritically ascribe phenomena in carbohydrate metabol-
ism to variations in the Embden-Meyerhof scheme." Cohen
(1955b) also suggests that at least six major pathways for glucose
metabolism are known and several may exist simultaneously in
the same organism.
When one considers the various animals and bacteria that have
been studied, it becomes quite clear that what we have so far
BASIC ASSUMPTIONS 11
examined is equivalent to a small drop in a very vast ocean. It is
pleasing that so much has already been discovered, but there is
very little doubt that there is a great deal yet to be discovered about
carbohydrate metabolism. It is therefore premature to claim that
the " universal " occurrence of the glycolysis and citric cycles
is proof of the common origin of life from one source.
To indicate some of the further biochemical complexities we
may briefly mention four points. Firstly, it is often stated that all
living systems use the same twenty or so amino-acids. This is
a simplification of the known data. At one time it was thought
that only the L-amino-acids occurred in natural systems, but
since then a few D-amino-acids have been isolated. The number
of known natural L-amino-acids has increased with the develop-
ment of chromatographic techniques. Meister (1957) quotes some
seventy naturally occurring amino-acids and he points out that
new ones are being discovered almost every month ! This is a
result of the application of new techniques to an extended range
of animal and plant material instead of restricting research to
mammalian tissues.
Secondly, there are a large number of bacteria that use aberrant
biochemical systems. Outstanding amongst these are the sulphur
bacteria which grow quite well on water, carbon dioxide, phosphate
and either sulphuretted hydrogen or sulphur. Another bacterium,
Thiobacillns ferro-oxidans, can in some cases grow on ferrous iron
under acid conditions which prevent the direct aerobic oxidation
of ferrous iron. Other bacteria take ammonia and dehydrogenate
it, or nitrite and oxidise it. There is some argument whether these
systems are primitive or whether they are advanced and overlaid
on the basic glycolysis and tricarboxylic cycles (see p. 22). These
examples indicate that the metabolic systems in the bacteria are
extremely varied.
Thirdly, even in the higher Metazoa the distribution of hydro-
gen acceptor systems such as in the cytochromes, flavoproteins,
tocopherols, vitamin K, etc., is no more uniform than the dis-
tribution of blood pigments we mentioned previously.
A fourth generalisation that has been made about protoplasm
is that its energetic systems involve the formation and destruction
of " high energy " phosphorus compounds and the ubiquity of
the phosphorus-containing compounds in living cells has been
12 BASIC ASSUMPTIONS
regarded as further evidence of a common protoplasmic origin.
At first it was thought that the " high energy " compounds were
found only in the form of ATP (adenosine triphosphate). But
further studies have since shown the existence of many other " high
energy ' nucleoside triphosphates, e.g. guanosine triphosphate,
cytidine triphosphate and uridine triphosphate. Recently other
1 high energy ' ' compounds have been discovered which contain
sulphur, i.e. acetyl coenzyme A. (Lynen 1952, Lipmann 1958). It
is possible that further " high energy " compounds will be dis-
covered in the future and this greater variety will make it less
obvious that all protoplasm uses the same energetic systems.
Thus on the biochemical side it seems premature to conclude
that all protoplasm has a common origin just because many
cells show the components of the glycolysis cycle, citric cycle and
the " high energy " phosphate compounds. It is likely that the
protoplasm of different animals will show the presence of other
schemes for the systematic degradation of carbohydrates and then
perhaps in time an analysis of these systems will allow us to come
to further conclusions about the varied metabolism of protoplasm.
Morphological evidence. A line of argument developed by
morphologists to show the common origin of living cells is the
almost universal occurrence of the mitotic and meiotic cycle. Thus
Grasse (1952) suggests that such a system indicates the mono-
phyletic origin of present-day animals and protozoa. But as
Boy den (1953) pointed out, the mitotic cycle is not so fixed or so
invariable as people imagine.
There are variations such as the presence or absence of intra-
or extra- nuclear spindles and the presence or absence of centrioles.
Thus Amano (1957) suggests that the chromosomes are separated
by extending fibres in animal cells though a different mechanism
exists in plant cells. On the other hand Swann (1951) suggests
that the chromosomes in the Arbacia egg separate because of the
contraction of fibres. In fact a perusal of Schrader's book Mitosis
(1953) makes it quite clear that one difficulty in finding a single
hypothesis to explain the mechanisms of mitosis in all cells is that
there are a large number of different mechanisms of mitosis. It
also seems that various tissues synthesise their DNA at different
stages of the mitotic cycle and that the chromosomes may be
duplicated at these various stages (Leuchtenberger 1958). It is
BASIC ASSUMPTIONS 13
possible that a more detailed examination of mitosis will show that
it too is a polyphyletic system devised for the successful separation
of the nuclear material into two equal sets. Whether one could go
as far as Boyden (1953) and say ,; Under the circumstances the
widespread occurrence of what is called mitosis or meiosis is no
proof of real genetic relationships of all such organisms. On the
contrary the very existence of such mechanisms in organisms
otherwise so diverse as Protista, Metazoa, and Metaphyta, is
strongly suggestive of convergence and may thus be interpreted
with the theory of the strictly polyphyletic origins of the major
groups of organisms " is another matter in our present state of
ignorance.
What then can one conclude about the chemical and physical
nature of protoplasm? Simply that we have a very great deal to
learn about it. Modern developments are making it abundantly
clear that some of our previous concepts are quite inadequate and
that the picture is very much more complex than previously
imagined. It would be a great mistake to assume that all is chaos
and that there are no general common systems, but it would be a
mistake of equal magnitude to assume that everything is very
simple and that but one system will be found in all protoplasm.
From our present viewpoint there would appear to be at least four
or five different systems which allow a cell to obtain its energy.
There are minor variations in this pattern and the higher animals
may show less variation than do the bacteria (though few higher
animals other than the pigeon and the rat have been studied).
The picture in no way allows us to dogmatise and state that life
in all its manifestations shows a common biochemical system
indicative of a single genesis. The evidence at present does not
by any means exclude the concept that present-day living things
have many different origins.
Polyphyletic origin of life
If we do not hold that the origin of life was unique, i.e. life is
monophyletic, there is the alternative point of view. This is that
living things have been created many times, i.e. polyphyletic.
There are two ways of considering the multiple origin of life.
The first is to consider that life is continuously being created all
the time, i.e. that spontaneous generation is always occurring. The
14 BASIC ASSUMPTIONS
second view is that spontaneous generation occurred at some
finite time in the past but that it is no longer occurring.
The continuous formation of life de novo. This theory is of
considerable antiquity and it might be as well to give a brief
resume of its history. The responsibility for it is usually placed
at the door of Aristotle. He wrote: " It is quite proved that certain
fish come spontaneously into existence not being derived from
eggs or copulation. Such fish as are neither oviparous nor
viviparous arise all from one of two sources, from mud or from
sand, and from decayed matter that rises hence as scum; for
instance the so-called froth of small fry comes out of sandy
ground. The fry is incapable of growing and of propagating its
kind, after living for a while it dies away and another creature
takes its place and so, with short interval excepted, it may be said
to last the whole year throughout."
Other biologists gave various recipes for the formation of life
de novo. Virgil in his Georgics, Book IV, gives the recipe for the
formation of a swarm of bees from the barren carcass of a dead calf.
Van Helmont suggested that mice could be formed " if a dirty
undergarment is squeezed into the mouth of a vessel, within
21 days the ferment drained from the garment and transformed by
the smell of the grain, envelops the wheat in its own skin and
turns into mice." Van Helmont was surprised that mice formed
in this manner could not be distinguished from mice produced by
normal sexual breeding.
The situation became more critical when the experimentalists
tried to determine whether it was possible to prevent living things
from appearing in preserved material. The experiments of
Needham, Pouchet and Bastian all indicated that living things
still appeared in solutions from which all previous life had been
removed, whilst Redi, Swammerdam, Vallisneri, Spallanzani,
Schwann, Pasteur and many others showed that if the experi-
ments were done very carefully it was possible to preserve soups,
blood or urine in an atmosphere of oxygen and still get no growth
of living material. It is not my intention here to discuss this old
controversy. Full and interesting details can be found in the books
of Oparin (1957), Singer (1950) and Wheeler (1939). Today
there are still people who think that living things of a high level
of complexity can be formed de novo. Of these it is perhaps of
BASIC ASSUMPTIONS 15
interest to quote from one Wilhelm Reich (1948). Reich has
developed the concept that living material accumulates units of
primordial energy which he calls " orgones." These orgones may
be taken up by small vesicles (bions) that exhibit certain similar-
ities to living material. By studying these bions and bion complexes
under the very high optical magnification of 5,000 times (" it is
not a matter of visualising finer structural detail but movement ")
Reich concludes that bacteria and Protozoa can arise from sterilised
organic and inorganic material. Thus from autoclaved grass he
observed the development of amoebae and other Protozoa. Reich
was not satisfied with the alternative explanation that the spores
might have been present in the grass since he had also obtained
similar amoebae from inorganic material such as sand or iron
filings placed in the sterilised medium! The bions give off
radiations which affect living material, and in some ways this
radiation resembles the mitogenetic radiation studied by Gurwitsch
(1926). It will be remembered that Gurwitsch claimed that the
mitogenetic rays which come off from living cells affect the division
rate of other cells. The experimental verification of mitogenetic
radiation has proved to be very difficult and at best inconclusive ;
the evidence is summarised in Hollaender and Schoeffel (1931)
and in Gray (1931), but as yet there has been no work on orgones
other than from Reich and his colleagues. The work of Reich is
of interest in that it shows that there are still " heretics " at work
on the age-old problem of the origin and nature of living organisms.
Joseph Needham, writing in his textbook Chemical Embryology
(1931) stated, " It may be remarked here, without irrelevance,
that the problem (of spontaneous generation) is still unsolved ; for
all that was proved by the experiments of Spallanzani was that
animals the size of rotifers and Protozoa do not originate spontane-
ously from broth, and all that was proved by those of Pasteur
was that organisms the size of bacteria do not originate de novo.
The knowledge which we have acquired in recent years of filter-
passing organisms such as the mosaic disease of the tobacco plant,
and phenomena such as the bacteriophage of Twort and d'Herelle
has reopened the whole matter, so that of the region between, for
example, the semi-living particles of the bacteriophage (10~15 g)
and the larger-sized colloidal aggregates (10~18 g) we know
absolutely nothing. The dogmatism with which the biologist of
16 BASIC ASSUMPTIONS
the early twentieth century asserted the statement omne vivum
ex vivo was, therefore, like most dogmatisms, ill timed."
The argument developed so far, then, is as follows. The
ancients thought that in many cases it was possible for living things
to be created de novo. All these cases depended upon poor
observation or lack of knowledge, and gradually as information has
become available all the higher animals have been shown to arise
from previous generations. The simpler forms of life such as
yeast and bacteria were at one time thought to arise spontaneously,
but controlled experiments showed that these observations were
at fault. The conclusion is thus that the onlv cases where we think
j
that life may be formed de novo are those where we have no
information as to the mode of origin. From this one might suppose
that spontaneous generation does not take place, but this is an
unjustified extrapolation. The correct extrapolation would be
that until we have devised experiments in which the simpler forms
of life, such as viruses, are developed de novo, we have no evidence
of de novo origin of life. This does not imply that de novo genera-
tion is or was impossible: Oparin (1957) suggests that life was
created de novo on this world at one time and it is possibly being
created now somewhere in the universe, but it is not being
created now in this world since the ubiquitous presence of living
bacteria would prevent the accumulation of the necessary raw
materials for the formation of life de novo. When life was first
created there were no such bacteria and hence the necessary
substances accumulated. If we accept Oparin's view that life is
not formed de novo at present in the world, there are still two
alternative suggestions concerning the origin of life. The first is
that life is still being formed de novo in other parts of the universe
and is then transmitted by meteorites to this planet. Ousdal
(1956) has described in meteorites some very interesting shapes
which in some ways resemble present-day living forms (Fig. 1).
However, the meagre evidence so far available that meteorites may
contain living material is not yet convincing. It should be noted
that the present climate of opinion concerning the possible
mechanism of the evolution of the present solar system is changing.
The view suggested by Sir James Jeans that the planets were
formed by the unique passage of a giant star near to the sun is
no longer strongly supported (Lyttelton 1956). Instead it seems
BASIC ASSUMPTIONS 17
that solar systems similar to our own have been created many
millions of times and thus conditions favourable to life may be
present on many other planets in the universe. Shapley (1957)
has calculated that there are probably 108 planets that have con-
ditions favourable for life of one sort or another. We have no
evidence that living things can be transmitted between the stars
and still remain alive on reaching their destination, but it would
seem that we shall shortly have information on transmission of
living material by rockets. It would perhaps be more to the point
to have information concerning transmission by meteorites.
Oparin (1957) gives quite an extended discussion of meteorite
transmission of life and concludes that it was, and still is, highly
improbable. Nevertheless, at present we have very little informa-
tion on this subject and it is likely that the renewed interest in
space travel will stimulate further investigation into the nature and
properties of meteorites.
Unique occurrence of life. The second suggestion is that
though we are unable to show at present that life is formed de
novo on this earth, there is no evidence to show that when life was
formed on this earth it was a unique event. Haldane (1954) and
Oparin (1957) are of the opinion that life was uniquely formed, but,
as they both point out, nothing is definitely known about what did
happen; all is hypothesis, and though it is simpler to assume
that it was a unique occurrence there is no reason why this simple
explanation should be the correct one. In the previous pages it
has been pointed out that our knowledge of the cell metabolism
is insufficient to allow us to state categorically that all cells in all
living forms have the same biochemical systems at work. Though
the similarities are often great, the dissimilarities may be just as
impressive.
If living material had developed on several different occasions
or at different places at the same time, then one would expect to
have a large number of distinct groups of animals, whose relation-
ships and affinities are difficult to determine.
This, as we shall see, is the present situation.
CHAPTER 3
VIRUSES, RICKETTSIAE AND BACTERIA
If one assumes that the origin of life was a unique occurrence
then it follows that all the present-day living things must be
derived from this original source. This then poses the problem,
" What is the relationship between the present-day forms? ' In
many cases it is difficult to form any definite conclusion
regarding these relationships and this certainly seems to
hold for the relationship between Viruses, Rickettsiae and
Bacteria.
The viruses
The viruses are of interest since they show many of the
properties of living material. At first they were described as
material that would pass through a bacterial filter and which wTas
capable of reproducing in the living cell. But later on consider-
able confusion arose over the chemical nature of viruses, the main
trouble being one of over-simplification. Many people thought
that the viruses were necessarily simple because they had been
prepared in a crystalline condition. This concept was furthered
when chemical analysis showed that the virus was composed
of a " simple chemical substance " — nucleoprotein. With more
advanced techniques it became clear that there was considerable
variability in virus structure. Markham, Smith and Lea (1942)
showed that when the tobacco mosaic virus was irradiated, only
a small part of the virus proved sensitive to radiation. This part
was some 5%-6% of the virus area and in effect it behaved like
the nucleus of the virus. In 1951 Markham and Smith presented
evidence that the turnip mosaic virus contained at least two
distinct components, a nucleic acid component (38%) and a
structural protein component (62%).
18
Fig. 2. Virus structure. The tobacco mosaic virus is made up from
at least two components. There is a central rod of nucleic acid and
a series of units of protein that fit over the central rod. In the
photograph shown here part of the second component has been
dissolved away to reveal the nucleic acid. (This photograph was
obtained through the kindness of Professor G. Schramm.)
Head
Contracted
sheath
r
ore
ft Plate
I art
fibre
Fig. 3. Virus structure — Bacteriophage. The Bacteriophage has a
more complex structure than a simple virus such as the tobacco
mosaic virus. It has a well-developed head and a tail. The head
contains the nucleic-acid component and this flows through the
tail into the bacterium it attacks and there reproduces. (This
photograph was obtained through the kindness of Dr. S. Brenner
and Dr. R. W. Home.)
Fig. 4. Bacterial structure. The bacterial cells have complex
structure as is shown by this electronmicrograph of a section
through B. cereus. The cells have a well-defined cell wall, a
nuclear structure, and many types of cell inclusions. (From
Chapman and Hillier.)
(A) Cell wall. (F) Fibrous material.
(C) Peripheral bodies. (G) Nucleus.
(D) Transverse cell wall. (H) Cytoplasm.
(E) Transverse cell wall. (|) Inclusions.
L.M.R. Limit of light microscope.
VIRUSES, RICKETTSIAE AND BACTERIA 19
Takahashi and Ishii (1953) showed that it was possible to find
the structural protein in the sap of the plants infected with the
mosaic virus and that it differed from the normal plant proteins.
This protein had no power of reproduction but required the
presence of nucleic acid. If the nucleic acid was added to the
structural protein, then it became capable of reproduction inside
the cell (Fraenkel-Conrat and Williams 1955).
The chemical analyses of virus structure have been paralleled
by studies using the electron microscope. These show that the
tobacco mosaic virus is often found in rod-like forms, the rods
being made up of a series of discs each with a hole in the centre.
The hole is apparently filled with the nucleic acid whilst the disc
itself is probably the structural protein (Fig. 2).
Other viruses such as bacteriophage which attacks bacteria
have an even more complex structure. The bacteriophage has a
tadpole-shaped head and a small tail (Fig. 3). The head consists
of a shell of structural protein inside which is the nucleic acid.
Hershey (1956) described how it was possible to remove the
nucleic acid from the bacteriophage and leave the tail and the
shell. This skeleton was still capable of attacking a bacterium
and killing it, but it was not capable of self-reproduction.
Detailed chemical analysis and electron microscope studies
have therefore shown that viruses are not simple single chemical
substances. There is a considerable range of structural and
chemical complexity within the group of viruses and it is possible
to draw up a table showing the differences in their chemical
composition.
Material Present Virus
RNA
DNA
Protein S- Animal virus
Fats
Carbohydrates J
i
RNA
DNA ?
Protein Y Bacteriophage
Fats
3— IOE
20 VIRUSES, RICKETTSIAE AND BACTERIA
Material Present Virus
RNA "|
DNA ^ Polyhedral virus
Protein J
Tobacco mosaic virus
RNA \
Protein j
RNA ?
Thus the analysis of the vaccinia virus shows the presence of
proteins, DNA, neutral fat, phospholipid, cholesterol, biotin,
flavine, copper and various as yet unidentified substances. The
Lee influenza virus has about 5% of its weight as a complex
polysaccharide containing mannose, galactose and glucosamine.
It is also becoming clear that the term " nucleic acid " should be
used with care since there are many different nucleic acids, and as
ChargafT (1957) points out, often the term " ribose nucleic acid "
is used when there is no evidence that the sugar ribose is present.
The precise structure of the nucleoproteins is not yet known, i.e.
the type of proteins, and the way in which the nucleic acid is
attached to the protein have yet to be fully elucidated, but some
evidence is available concerning the component nucleotides in the
nucleic acids of the virus. The table below, taken from Fruton
and Simmons (1958) indicates that the proportional composition
of the nucleotides varies in the different viruses.
Virus Molar proportions in nucleic acid
Adenylic Guanylic Cytidylic Uridylic
acid acid acid acid
Tobacco mosaic virus 1-0 0-89 0-65 0-88
Cucumber mosaic virus 1-0 1-0 0-75 1-15
Tomato bushy stunt
virus 1-0 10 0-74 0-89
Turnip yellow mosaic
virus 1-0 0-76 1-68 0-98
This gives some hint of the complexity of nucleic acid, and
nucleoprotein structure, and makes one careful when ascribing
simplicity to a system that is not yet adequatel)' understood.
VIRUSES, RICKETTSIAE AND BACTERIA 21
There are two main views concerning the nature of viruses. One
suggests that they are in fact the simplest and most primitive
forms of living material and that originally they utilised the pro-
teins found in the complex primaeval " soup." As they gave rise
to more complex living things which altered and destroyed the
primaeval soup, so they became obligate parasites in other living
systems that evolved along different lines. On the other hand there
is the view that the viruses arose from more complex systems and
that in effect they are more like genes that have taken on a free-
lance life. Both of these views are discussed by Luria (1953).
There are other opinions concerning the nature of viruses. Thus
Hadzi (1953), for example, has suggested that viruses are the
spores of parasitic Protozoa. It is possible that all these opinions
are correct and that the viruses are a complex group of substances
at present classified by their properties and that these properties
depend on the level of organisation that has been achieved. The
viruses are thus most likely a grade of organisation that has been
reached from many different directions.
In this context and throughout the book, a grade may be re-
garded as a group of individuals that are united by certain common
properties but are not derived from a common close ancestor.
The grade indicates the level of organisation rather than a close
phylogenetic relationship.
The rickettsiae
The rickettsiae cause such diseases as typhus, murine fever and
spotted fever. They have properties between those of bacteria
and viruses; they approach the bacteria in structural complexity
and size, and they resemble viruses in that they are unable to
reproduce outside living cells (though this is not a stringent
criterion; it merely indicates lack of experimental success so
far).
The rickettsiae are more complex than viruses in that they are
able to carry out certain of the metabolic processes of the higher
cells. Thus they are capable of oxidising glutamate, pyruvate,
succinate, fumarate and oxalo- acetate. These substances are also
oxidised by the mitochondria of the normal cell, and the sug-
gestion has been made that the rickettsiae are in fact free mito-
chondria. Thus both the mitochondria and rickettsiae lose their
22 VIRUSES, RICKETTSIAE AND BACTERIA
diphosphopyridine nucleotide and coenzyme A on freezing, the
freezing in some way affecting the properties of the membrane
around the rickettsiae or mitochondria. It is possible that the
rickettsiae are developed as free mitochondria and that the viruses
are further simplifications. On the other hand the rickettsiae
may indicate a stage in the development of the viruses to bacteria
or the three groups could be quite unrelated.
We have insufficient evidence as yet to come to any firm con-
clusion concerning the origin and affinity of the rickettsiae.
Bacteria
We are no wiser when we come to consider the status of the
bacteria. Within recent years there has been a considerable
increase in our knowledge of the structure of the bacterial cell
(Spooner and Stocker 1956; Zinsser 1957). Thus Robinow in 1946
suggested that there were certain components within the cells of
Escherichia coli that behaved like nuclear material during cell
division (Fig. 4). Lederberg (1947) showed that a type of crossing
over occurred between certain strains of E. coli and that in effect
it was possible to draw up a map of the positions of various factors
in bacterial metabolism. The conclusion, then, is that certain
bacteria show nuclear and sexual (parasexual) behaviour. On the
other hand there are many bacteria that do not show these
phenomena, their structure and life history being much more
simple.
It is not clear whether the bacteria represent an evolutionary
approach to the Protozoa, whether they are a retreat from the
Protozoa or whether they are quite unrelated. Perhaps some of the
difficulties can be illustrated by considering the autotrophic
bacteria (Chemoautotrophic) (Fry and Peel 1954). These
bacteria such as the sulphur and iron bacteria are able to metabolise
various simple substrates. They raise the question " are these
bacteria using a more primitive (earlier developed) system than
those found in the heterotrophic and photosynthetic bacteria? '
It is not possible to give a definite answer to this question since
our knowledge of the biochemistry of the heterotrophic and
chemoautotrophic bacteria is still very incomplete. The chemo-
autotrophs can obtain their energy from simple sources such as
hydrogen, methane, ammonia, nitrite, hydrogen sulphide or iron
VIRUSES, RICKETTSIAE AND BACTERIA 23
compounds. These substances are very much less complex than
the carbohydrates from which the higher animals obtain their
energy. The simple hypothesis is that the chemoautotrophs are a
side-line representing a more primitive state of development than
that shown by heterotrophic and photosynthetic bacteria. Though
this opinion is quite widely held, evidence is gradually accumula-
ting to indicate the opposite view; viz. that the chemoautotrophs
are in fact using systems that are secondarily simplified from those
of the heterotrophs. Thus O'Kane (1941) showed that the
sulphur bacterium Thiobacillus thioxidans could synthesise various
vitamins of the B group. These substances are used mainly in
normal heterocyclic heterotrophic glycolysis; thiamine is used in
oxidative decarboxylation; riboflavine is a coenzyme for the
hydrogen acceptors, nicotinic acid forms part of Coenzymes I
and II. It would therefore be interesting to know what role they
plav in Thiobacillus. It would appear that the bacterium has many
of the enzymes that are used in heterotrophic glycolysis but that
it uses special variations on the normal system. The chemo-
autotrophs would then have superimposed their own system upon
that of the heterotrophs.
A schematic system for the development of metabolic systems is
shown below. If this is correct, and the chemoautotrophs are
less primitive than the heterotrophs, it again points the lesson
that the simplest explanations are not necessarily the correct
ones.
Scheme for the origin of metabolic systems (after Oparin) :
(1) Solution containing salts.
(2) Solution containing salts and simple organic compounds.
(3) Solution containing salts, simple and complex organic
compounds.
(4) System that turns complex materials into simple organic
materials and so obtains energy. Also able to reproduce
itself '■= a living system.
HETEROTROPHS (only glycolysis cycle)
(5a) Living system that converts complex organic material to
simple material.
HETEROTROPHS (glycolysis and citric cycles.
Hydrogen acceptors)
24 VIRUSES, RICKETTSIAE AND BACTERIA
(5b) Living system that converts simple material to obtain
energy.
CHEMOAUTOTROPHS (attack H2S,CH4, etc.)
(5c) Living system that develops PHOTOSYNTHESIS.
(Note that animals can by chemical means build up C02
to form carbohydrates.)
Bacteria and Protozoa
It is problematical how, if at all, the Bacteria are related
to the Protozoa and, if so, which Bacteria gave rise to which
Protozoa.
Grasse (1953) thinks that the Protozoa are in fact monophyletic
and derived from the Bacteria. He bases this opinion on the
following resemblances between the Protozoa and Bacteria.
(1) Both have vacuoles.
(2) Both contain proteins, lipids and carbohydrates.
(3) Both have mitochondria.
(4) Certain bacteria have a nucleus and chromosomes.
(5) A sexual process has been described in some bacteria.
(6) Both can possess flagella.
(7) Spore formation occurs in both.
(8) The membranes around the cell in each case are sometimes
morphologically similar.
These resemblances are rather tenuous and not all apply to any
one bacterium. In effect it is difficult to know to what extent the
resemblances are real phylogenetic ones and to what extent they
have risen by convergence. Thus the bacterial flagellum is very
much more simple in structure than the protozoan flagellum. The
protozoan flagellum has an inner strand of two rods and an outer
ring of nine rods. The bacterial flagellum has just the inner
strand of one or two rods. Until we know a great deal more
about the electron microscopy of the bacterial and protozoan cells
we shall not be in any position to base relationships on morpho-
logical similarities.
The relationship between Bacteria, Protozoa and Metazoa has
been discussed by Grasse, who derives the following alternative
systems :
VIRUSES, RICKETTSIAE AND BACTERIA
Autotrophic bacteria ->- Protophyta ->Metaphyta
(i) i _ i
Heterotrophic bacteria Protozoa — > Metazoa
25
(2)
Autotrophic bacteria -> Protophyta -> Metaphyta
Heterotrophic bacteria -> Protozoa -> Metazoa
Autotrophic bacteria Protophyta ->- Metaphyta
(3) I t
Heterotrophic bacteria — > Protozoa ->■ Metazoa
Autotrophic bacteria -
(4) }
Heterotrophic bacteria — > Protozoa
Protophyta ->■ Metaphyta
— > Metazoa
Grasse suggests that the first system is the most probable but that
all the others have something to be said in their favour. On the
other hand Oparin (1957) thinks that the heterotrophic bacteria
are the most primitive and that they gave rise to the autotrophic
forms and to the Protozoa and Protophyta, a view that is not
mentioned in Grasse's scheme. It can be seen that nothing is
definite ; all is hypothesis and opinion.
At present the following schemes all seem equally likely:
(1) The Bacteria and the Protozoa had an independent
phylogenetic origin.
(2) The Bacteria are more primitive than the Protozoa and gave
rise to the Protozoa.
(3) The Bacteria are secondarily simplified and were derived
from the Protozoa.
(4) The Bacteria are a polyphyletic grade. Some are more
primitive than the Protozoa, others are derived from the
Protozoa.
We have at present insufficient evidence to enable us to choose
between these hypotheses.
CHAPTER 4
THE PROTOZOA
We have just seen that the relationship between the simplest
living forms, the Viruses, Rickettsiae and Bacteria, is not at all
clear. We cannot say with any certainty how they have evolved
and what the relationship is between the three groups. When we
come to consider the next group of animals, the Protozoa, we shall
find a very similar situation. There is great difficulty in deciding
where the Protozoa came from, what they gave rise to, and what
their interrelationships are. The Protozoa can be classified into
four classes. These are:
(1) Flagellata; e.g. Chlamydomonas, Trichonympha.
(2) Rhizopoda; e.g. Amoeba, Elphidium.
(3) Sporozoa; e.g. Monocystis, Plasmodium.
(4) Ciliophora; e.g. Paramecium, Entodinium.
There are several evolutionary problems to be found in the
protozoans but only three of these will be considered here. The
first problem is, " Which of the four classes is the most primitive? '
The second problem is, " What is the interrelationship of the four
classes? " and the third problem is, " What is the status of the
group Protozoa? ' These problems will each be examined in turn.
The Most Primitive Protozoa
We can readily dismiss two of the four classes of the Protozoa
as candidates for the position of the most primitive class. The
Sporozoa are almost entirely parasitic in the bodies of higher
animals and they spend their life in the outside world in the
encysted state. Though it is possible that they could have arisen
in the " primaeval soup " that gave rise to living forms, their life
26
THE PROTOZOA 27
cycles are so involved and their structure with myonemes and spore
cases so complex that they are probably not very close to the
primitive stock. It is worth noting here that some authors such as
Ulrich (1950) have suggested that the Cnidosporidia are not
protozoans but metazoans.
The Ciliophora too can be disregarded since they show par
excellence the extremely complex structures that can exist within
the protozoan cell. Thus Entodinium with its complex cirri,
neuromotor system, skeleton, nuclei and digestive system is
almost as complex as some metazoans (Fig. 5). On the other hand
even the most simple of the ciliophorans have a complex nuclear
structure. There is usually a macro- and a micro-nucleus as
separate bodies, though they are in the form of macro- and micro-
chromosomes in a single nucleus of the Chonotricha such as
Spirochona. In addition there is the very complex infraciliature
that has developed in the superficial regions of the ciliates and
this is more complex than that found in the flagellates.
This then leaves two classes, the Flagellata and the Rhizopoda,
as the more primitive protozoans and each of these has at various
times been considered as the most primitive Protozoa. Thus at
the beginning of the century the prevalent view was that the
Rhizopoda were the most primitive of the Protozoa. This view
was well expressed by Ray Lankester (1890) in his article in the
Encyclopaedia Britannica. Lankester said, ' Briefly stated the
present writer's view is that the earliest protoplasm did not
possess chlorophyll and therefore did not possess the power of
feeding on carbonic acid. A conceivable state of things is that a
vast amount of albuminoids and other such compounds had been
brought into existence by those processes which culminated in the
development of the first protoplasm, and it seems therefore likely
enough that the first protoplasm fed on these antecedent steps in
its own evolution just as animals feed on organic compounds at
the present day, more especially as the large creeping plasmodia of
some Mycetozoa feed on vegetable refuse. It is indeed not
improbable that, apart from their elaborate fructification, the
Mycetozoa represent more closely than any other living forms the
original ancestors of the whole organic world. At a subsequent
stage in the history of this archaic living matter chlorophyll was
evolved and the power of taking carbon from carbonic acid. The
28
THE PROTOZOA
Motorium |
dorsal disc
Mouth
Frontal membranellae—
Contractile vacuole
Meganucleus'
Micronucleust
Cuticl
Ectoplasm
Contractile vacuole-
oral cirri
oesophagus
retractor fibres
Endoderm
Food vacuoles
- Caecum
- Retractor fibres
Anus
Fig. 5. Protozoan structure. — Entodinium. This is a complex
ciliate and has much of the differentiation that one expects to
find in the higher animals. Thus it has a mouth, gullet, cloaca,
myonemes, neuronemes, contractile vacuoles, skeletal system and
several nuclei. (After C. V. Sharp.)
THE PROTOZOA 29
1 green ' plants were rendered possible by the evolution of
chlorophyll, but through what ancestral forms they took their
origin or whether more than once, i.e. by more than one branch,
it is difficult even to guess. The green Flagellate Protozoa
(Volvocinae) certainly furnish a connecting point by which it is
possible to link on the pedigree of green plants to the primitive
protoplasm; it is noteworthy that they cannot be considered as
very primitive and are indeed highly specialised forms as compared
with the naked protoplasm of the Mycetozoon's plasmodium.
Thus we are led to entertain the paradox that though the animal is
dependent on the plant for its food yet the animal preceded the
plant in evolution, and we look among the lower Protozoa and not
among the lower Protophyta for the nearest representatives of that
first protoplasm which was the result of a long and gradual
evolution of chemical structure and the starting point of the
development of organic form."
If one consults any of the older texts such as those of Lankester
(1909), Delage and Herouard (1896) or Kukenthal and Krumbach
(1923) one finds that the Rhizopoda are placed as the first class of
the Protozoa.
The accent of protozoan research changed during the first
part of the twentieth century. Instead of being concerned with the
morphology and life cycles of the Protozoa, the interest became
more centred upon the physiology and in particular the nutritional
requirements of the Protozoa. This change in accent from a
morphological one to a physiological one may explain the change
that took place in the prevalent attitude to the phylogeny of the
Protozoa. In such texts as those of Hyman (1940) or Grasse
(1952) the Flagellata take pride of place over the Rhizopoda; the
Flagellata being the first class to be described. It should, however,
be noted that Klebs in 1892 suggested that the Flagellata were in
fact more primitive than the Rhizopoda.
Grasse points out that since many of the members of the
Flagellata possess chlorophyll they are able to undertake synthesis
of all their food requirements without the assistance of any
complex compounds. This view is much the same as that of
Pringsheim (1948), who showed that many of the colourless
flagellates such as Astasia or Polytoma can be found in pure
cultures of Euglena and Chlamydomonas respectively. The
30 THE PROTOZOA
coloured forms gave rise to the colourless forms, i.e. Astasia is a
colourless Euglena, and hence the groups Astasia and Polytoma
are not strict monophyletic genera but instead are polyphyletic
grades. Pringsheim suggests that many of the present-day colour-
less flagellates are derived from the coloured form and this would
make the coloured forms more primitive than the colourless forms
(Pringsheim and Hovasse 1950).
Lwoff (1944) in his book on physiological evolution goes even
further and contends that from a physiological point of view
evolution is retrogressive. The most primitive Protozoa, he states,
must surely have been entirely self-supporting with little or no
food requirements, but as evolution occurred the cells lost their
synthetic ability and became more and more dependent upon other
cells for the provision of their food requirements; i.e. they
regressed instead of progressed.
There appears to be a fallacy in LwofT's argument. The fact
that a cell has minimal food requirements does not mean that this
is necessarily the most primitive condition. In fact most of the
schemes suggested for the origin of living material place the
advent of chlorophyll at a very late stage in the evolutionary
sequence, the plant cells having the chlorophyll system super-
imposed on the anaerobic metabolic system (Oparin 1957). The
very earliest living forms would have had considerable food re-
quirements. It would be perfectly possible for a sarcodine-like
form to be the most primitive animal feeding on amino-acids and
carbohydrates synthesised by abiogenic methods. The presence
of chlorophyll is indeed a good reason for considering the Flagellata
as an advanced group of the Protozoa. This view was in fact
suggested by Lankester in 1909.
Lankester stated, " The real question ... is whether we find
reason to suppose that the combination of carbon and nitrogen
to build up proteid, and so protoplasm, required in the earliest
state of the earth's surface, the action of sunlight and the chloro-
phyll screen. We must remember that these are now necessary
for the purpose of raising carbon, and indirectly nitrogen, from the
mineral resting state to the high elaboration of the organic molecule,
yet it is, after all, living protoplasm which effects this marvel with
their assistance ; and it seems (though possibly there are some who
would deny this) that it is protoplasm which has, so as to speak,
THE PROTOZOA 31
invented or produced chlorophyll. Accordingly I incline to the
view that chlorophyll as we now know it is a definitely later
evolution — an apparatus to which protoplasm attained, and as a
consequence of that attainment we have the arborescent, filamentous,
foliaceous, fixed series of living things we call plants. But before
protoplasm possessed chlorophyll it had a history. It had in the
course of that history to develop the nucleus with its complex mecha-
nism of chromosomes, and it had during that period to feed."
There is a second reason why the Flagellata are sometimes
considered to be more primitive than the Rhizopoda. During their
young stage some of the Rhizopoda such as Naegleria and
Dimorpha show a flagellate condition which is considered by some
investigators to be a form of recapitulation; i.e. the young stage
shows more primitive characteristics than those present in the
adult. How much faith can one have in this type of argument?
We know that certain flagellates such as Mastigamoeba show
pseudopodia as well as flagella and thus the presence or absence of
pseudopodia or flagella does not necessarily indicate primitive-
ness. What is more important is the concept that these Rhizopoda
show the flagellate stage only in the young forms and that there-
fore the flagella are more primitive than the pseudopodia.
We are lucky in that there has been a recent investigation by
Willmer (1956, 1958) into the factors that determine the acquisi-
tion of flagella by the amoeba Naegleria gruberi. Willmer showed
that the amoeboid Naegleria can be made to turn into a flagellate
form with one to four flagella by placing it in water. The change
takes from 20 min to 24 hr to complete and during this time
is accompanied by the development of a definite antero-posterior
axis in the cell; the flagella appearing at the anterior end. The
pseudopodia can develop from any part of the animal. The
presence of salts such as lithium chloride, magnesium chloride
and magnesium sulphate suppress the development of the
flagella but leave the pseudopodia fully active. The change from
amoeboid to flagellate condition is reversible and depends upon
the environmental conditions (Fig. 6). This means that the
flagellate condition is not necessarily found in the young animal ;
either stage can reproduce and either stage can be found in the
young animal. Bunting (1926) showed that the rhizopod Tetramitus
could undergo cell division in either the amoeboid or the flagellate
32
THE PROTOZOA
Fig. 6. Naegleria gruberi. This protozoan can exist in either of two
forms: an amoeboid form or a flagellate form. Stages 1-8 show-
stages during which the amoeboid form changes into the flagellate
condition. The arrow indicates the direction in which the animal
moves. (From Willmer.)
stage. This too indicates that the flagellate stage is not necessarily
the more juvenile one.
On the basis of this evidence we are left undecided as to which
is the most primitive, the Flagellata or the Rhizopoda. This
question will be dealt with again on p. 33, where a third inter-
pretation wrill be presented. In effect this third view states that the
Rhizopoda and Flagellata are not strict classes of the Phylum
Protozoa. Instead they are polyphyletic grades. The Flagellata arose
on many separate occasions from the plants, fungi and metazoa, and
the Rhizopoda developed in much the same manner. Both these
groups are then more in the nature of horizontal grades than vertical
monophyletic classes, one of which is older than the other.
Protozoan Phylogeny; the Interrelationship
of the Four Classes of Protozoa
The precise relationship of the four classes of Protozoa is
uncertain. The two classes that appear to be the most closely
related are the Flagellata and the Rhizopoda. Butschli in 1883
THE PROTOZOA 33
suggested that it was possible to derive these two classes from
intermediate forms such as Mastigamoeba, and this view has been
followed by Grasse in his Traite de Zoologie, where he groups the
Flagellata and the Rhizopoda into a subphylum : the Rhizoflagellata.
To the groups Flagellata and Rhizopoda he gives superclass status
and groups such as the Dinoflagellata and the Foraminifera are
termed Classes.
The Sporozoa were linked by such workers as Doflein (1916)
with the Flagellata and the Rhizopoda to form the group Plasmo-
droma. There are certain resemblances between these groups.
Sporozoans such as Plasmodium have both flagellate sperm and
amoeboid ookinetes, and spore formation is found in both the
Flagellata and the Rhizopoda. The Plasmodroma are then
separated from the Ciliophora with their complex infraciliature.
Yet even within the Ciliophora there are forms that are possibly
related to or have something in common with the Flagellata. Thus
Opalina is according to some writers a ciliate and according to
others such as Grasse it is a flagellate.
Such close connexions between the four classes can be inter-
preted as showing how closely the various groups are related. But
there is another interpretation. Franz (1924) has suggested that
the Protozoa are not a strict phylum but instead are a grade of
organisation. He thinks that there is no good evidence that the
Protozoa are more primitive than the Metazoa and states that
the unicellular forms could have been derived many times from
the Fungi, Algae and the Metazoa. The various groups such as the
Flagellata, Rhizopoda, Sporozoa or Cilophora would then each be
polyphyletic and contain animals that have been derived from
different sources at different times but which are grouped together
because they have certain convergent morphological characteristics.
The view that the four classes are polyphyletic is discussed by
Hyman (1940). " The flagellates themselves appear to be a hetero-
geneous assembly of groupsthat have probably arisen from a number
of different sources, possibly bacteria and spirochaetes, many of
which are provided with flagella. . . . The rhizopods like the
flagellates constitute an arbitrary assemblage of forms having in
common the pseudopodial method of locomotion and food capture.
It is probable that the various orders of rhizopods have arisen inde-
pendently from the different groups of flagellates, i.e. the class is
34
THE PROTOZOA
Dincclonium
(A)
(B). Gymnodinium
Fig. 7. Relationship between the Protozoa and Algae. The alga
Dinoclonium has a flagellate spore that resembles a dinoflagellate
such as Gymnodinium. It is suggested by some authors that
Gymnodinium is more closely related to Dinoclonium than it is to,
say, Amoeba. (From Grasse.)
THE PROTOZOA 35
polyphyletic. . . . The Sporozoa are again a heterogeneous group of
which the different orders have probably had separate origins. . . .
The Ciliata differ so markedly from the other Protozoa in their
possession of cilia, nuclear dimorphism, and sexual phenomena
that their relation to them remains problematical."
So of the four classes of the Protozoa we see that at least three
are suggested by Hyman as being polyphyletic.
Baker (1948) has similar doubts about the status of the Protozoa.
In particular he considers the relationship of the din ofl age 11 ate
Gymnodinium with the filamentous alga Dinoclonium (Fig. 7).
During the life cycle of Dinoclonium it develops spores almost
indistinguishable in structure from Gymnodinium, but Dinoclonium
is placed in the Algae whilst Gymnodinium and Amoeba are placed
in the Protozoa. The structure of these spores clearly shows that
Gymnodinium is more closely related to Dinoclonium than it is to
Amoeba. Baker concludes that the Protozoa cannot be a mono-
phyletic group.
From the evolutionary point of view we therefore have several
problems in the Protozoa.
(1) The Protozoa do not seem to be a group of closely related
animals. It is most likely that they are a polyphyletic group and the
name " Protozoa " indicates a grade or status rather than a
natural taxonomic group. In this they would be analogous to the
group " Vermes " or " Pisces " ; i.e. they show a level of organisa-
tion and not an evolutionary relationship. (We shall see that this
problem arises again and again; many of our phyla and classes are
grades of animals that are not closely related.)
(2) It is difficult to decide which of the Protozoa are the most
primitive. The information at our disposal is not sufficient to
allow us to come to any definite conclusion.
(3) Each of the four classes probably contains the results of
convergent development from heterogeneous stocks.
4— IOE
CHAPTER 5
ORIGIN OF THE METAZOA
When the basic assumptions underlying evolution were dis-
cussed on p. 13 it was pointed out that if the modern living forms
were polyphyletic, it should prove difficult to decide their inter-
relationships and we should have a number of isolated groups of
animals. This is precisely what we have discovered so far. The
Viruses, Rickettsiae, Bacteria and Protozoa are all quite distinct
from one another and their interrelationship is anything but
clear and certain. We come now to the Metazoa and we have to
decide whether they can be linked to any of the lower groups of
animals.
There are three main views concerning the origin of the
Metazoa. These are that the Metazoa arose from (1) the colonial
protozoans, (2) the syncytial protozoans, and (3) the Metaphyta.
Let us consider each of these views in turn.
(i) Origin from colonial Protozoa
Though the Protozoa are often defined as unicellular animals
there are many protozoans which after division or budding do not
separate their progeny so that the adult develops a colonial or
multicellular form. This development into colonies has taken place
many times within the Protozoa, as can be seen by looking at the
various classes. The most common examples are found in the
Flagellata. Simple unicellular forms such as Chlamydomonas can
at times exhibit an aggregated stage. An example of this is the
palmella stage during which Chlamydomonas encysts and divides
asexually ; the results enclosed in a gelatinous case may be regarded
as a colonial form (Fig. 8).
In Gonium sociale a group of sixteen Chlamydomonas like
individuals are associated together in a plate. All these forms are
36
ORIGIN OF THE METAZOA
37
(A). Chlamydomonas
Fig. 8. (A) Palmella stage of Chlamy-
domonas. During this stage the proto-
zoan divides but the cells remain
together enclosed in a gelatinous case.
The stage is " multicellular " though
it is in fact a resting stage in the life
history of the protozoan. (FromGrasse
after Goroshankin.)
Haematococcus
Fig. 8. (B) Palmella stage of
Haematococcus. (From Grasse
after Wollenweber.)
alike and at reproduction each of them divides and forms gametes.
A more complex colony is that of Eudorina in which there are
sixty-four individuals (Fig. 9).
Pleodorina illinoiensis and Pleodorina californica show further
stages in the development of the colony in that a group of cells
become differentiated from the others and they are unable to take
part in reproductive activities. There are four somatic cells in
Pleodorina illinoiensis and thirty-two in Pleodorina californica.
The soma is even more developed in Volvox, where the majority
of the cells are unable to take part in the reproductive activity. The
cells beat their flagella in a co-ordinated manner so that the
colony can be regarded as having an antero-posterior axis and a
dorso- ventral axis. The dorsal cells are slightly larger than the
ventral cells and the colony during locomotion moves slowly
through the water and does not turn over and over (Fig. 10).
38
ORIGIN OF THE METAZOA
(A). Gonium pectorale
(B). Eudorina illinoiensis
Fig. 9. Colonial flagellates. Flagellates such as Gonium and
Eudorina exist in a colonial form. The colony is active and thus
differs from the palmella stage shown in Fig. 8.
(A) From Grasse after Migula. (B) From Grasse after Merton.
ORIGIN OF THE METAZOA
39
(A). Dorsal View
(B). Side View
Fig. 10. Colonial flagellates. Volvox though a colonial animal has
protoplasmic connexions between the units of the colony. In this
respect it can be regarded as a syncytium. (From Borradaile and
Potts, after Janet.)
40
ORIGIN OF THE METAZOA
These examples are merely illustrative phases of the develop-
ment of the colonial habit. There is no evidence that Eudorina
gave rise to Pleodorina or Volvox.
Further examples of the development of colonial stages are
found in the dinoflagellates. Though some forms such as
Gymnodinium are solitary, others such as Ceratium at times may
form long chains of individuals joined together in a temporary
manner. Polykrikos is of interest since it shows a more permanent
attachment. Polykrikos schwartzi usually contains four nuclei and
a series of associated sets of flagella. It possesses cnidocysts which
are manufactured within the cell and are used in catching prey.
There is also a cytoplasmic connexion between the units of the
Polykrikos colony. Thus in the related genus Pheopolykrihos
beauchampi when the animal is touched it contracts up and
clearly shows that there are four units in interconnexion
(Fig. 11).
(A). Normal Animal
(B). Diagram of shape of animal aftertactilestimulation
Fig. 11. Colonial dinoflagellates. The dinoflagellate Pheopolykrikos
is clearly made from four dinoflagellate units. When it is touched it
changes its form (B) and the four units can be distinguished. (From
Grasse after Chatton.)
ORIGIN OF THE METAZOA 41
Another interesting colonial dinoflagellate is the parasitic form
Haplozoon. This is found in the gut of polychaetes. It forms
first of all a small cell which attaches to the gut of the host by
means of a spike and some filamentous pseudopodia. This cell
absorbs food from the polychaete and at a later stage divides.
The results of division do not detach but instead remain in contact
so that a colonial form of up to several hundred cells is soon
formed, the number of cells differing from species to species.
These cells can form a three-dimensional mass with small spaces
between the cells through which food particles can be transferred
(Fig. 12).
Fig. 12. Colonial dinoflagellates. Haplozoon was originally placed
in the Mesozoa but its spores have typical dinoflagellate structure
and it is now considered to be a colonial dinoflagellate. (From
Grasse after Dogiel.)
The relationship of Haplozoon to the Dinoflagellata is not
clear at first sight. In fact Haplozoon is so much like a metazoan
that when it was discovered by Dogiel in 1906 he placed it in the
Catenata, a new group of the Metazoa. It was not until the work of
Chatton (1920) that it was shown that the cells at the posterior
end of Haplozoon detached and developed into four small spores,
each of which had characteristic dinoflagellate structure. It is for
this reason that Haplozoon is placed in the Dinoflagellata. This
reasoning can, if carried to its illogical conclusion, lead one into
difficulties. Thus Duboscq and Grasse (1933) have shown that
the mammalian spermatozoan is very much like a protozoan of the
group Bodoines, yet I doubt if anyone would like to place Man in
the Protozoa on account of his male gamete !
Colonial Protozoa are also found in the other classes. In the
Ciliphoroa, Anoplophrya forms chains of cells, whilst Carchesium
and Zoothamnion form branching colonies (Figs. 13 and 14).
In Zoothamnion the myonemes run throughout the length of the
colony so that if one part contracts then all the rest contracts. In
Carchesium the myonemes are restricted to each unit so that they
42
ORIGIN OF THE METAZOA
Fig. 13. Colonial ciliate. Zoothamnion shows a differentiation of its
parts so that there are feeding zoids and reproducing zoids. In many
respects it appears similar to a colonial coelenterate. (From Hyman.)
ORIGIN OF THE METAZOA
43
-LI '.':/ I I U.
Fig. 14. Colonial ciliates. Anoplophrya is colonial only in that the
cells formed by asexual division often remain attached in the form
of a chain. (From Borradaile and Potts.)
contract individually. Zoothamnion is of interest in that it shows
considerable variation in the structure of its units, the colony
showing division of labour (Faure-Fremiet (1930); Summers
(1938)).
Colonies are found in the cnidosporidian Sporozoa, the spores
showing well-marked differentiation into cnidocysts each with its
own nucleus, a spore nucleus and a spore case nucleus (Fig. 15).
Whether it is justifiable to regard these reproductive units as
Fig. 15. Colonial sporozoa. The spores of the Cnidosporidia have
a complex structure, (a) Shows the adult trophozoite and it will
be seen to resemble the trophozoite of other sporozoans such as
Monocystis. (b) Spore case together with the undischarged thread
cells, (c) Spore case with discharged thread cells.
(a) Sinuolenea. From Grasse after Davis.
(b) Myxobolus. From Grasse.
(c) Chloromyxum. From Grasse after Kudo.
44 ORIGIN OF THE METAZOA
colonial forms is not clear. Baker (1948) and Ulrich (1950)
suggest that the Cnidosporidia may be degenerate Metazoa but
since complex spores are also found in other Sporozoa, e.g. the
cysts of gregarines, and since the sporozoite of the Cnidosporidia
is very similar in structure to that of Monocystis, it is more likely
that they are real sporozoans and not degenerate Metazoa (Fig. 16).
Under certain conditions the rhizopod Naegleria can aggregate
so that the cells being joined by a sticky material form a sheet of
tissue (Willmer 1956). Sphaerozoum is another colonial rhizopod
— a radiolarian — and in the Mycetozoa there are many forms that
show colonial structure at certain stages of their life history. What
is of interest here is that colonies such as Dictyostelium have
developed a chemical system that keeps the amoebae that go to
make up the colony in a unit (Bonner 1949). In general the
Rhizopoda tend to form syncytia more easily than they form
colonies. On the other hand quite complex multilocular skeletons
are found in the Foraminifera, but there is usually only one living
cell present.
From the foregoing account it is evident that the Metazoa could
have arisen from the colonial protozoans. There are a large
number of colonial Protozoa and many of them show differentia-
tion and division of labour amongst the colony. Whether the
Metazoa did in fact arise from the colonial protozoans is another
matter and we must now consider the alternative theories.
(2) Origin from a syncytial cell
This theory suggests that the origin of the Metazoa must be
sought from a protozoan that had many nuclei and which later
developed membranes separating these nuclei off. The syncytium
differs from the colony in that the primary unit is the whole
animal and that it later becomes multicellular. In the colony the
primary unit is the cell and many of these units come together to
form the animal.
The differences between the syncytium and the colony are not
as clear cut as could be desired. In the main they depend upon
the absence of cellular boundaries. But what does one say in the
case of Volvox or Pheopolykrikos where there is protoplasmic
connexion between the cells (Figs. 10 and 11). Is this a multi-
cellular animal or a syncytium?
ORIGIN OF THE METAZOA
45
.•••I.C-'-'V ••.'"■ .■'N-
Fig. 16. Sporozoan structure. Spore cases of gregarines. The
Cnidosporidea are not the only forms to have complex spore cases ;
the gregarines have them too. (a) shows the complete spore case,
(b) shows details of the tube through which the spores are dis-
charged, (c) shows the tube everted and the spores being discharged
through it. Such a reproductive spore case with its evertible tubes
has something in common with the spore case of the Cnidosporidea.
(a) Gregarina munieri after Schneider, (b and c) Gregarina ovata
after Schnitzler. (Both from Grasse.)
46 ORIGIN OF THE METAZOA
Baker (1948) suggested that since in his definition a cell is "a
mass of protoplasm largely or completely bounded by a membrane
and containing within it a single nucleus formed by the telophase
transformation of haploid or diploid set of anaphase chromosomes,"
that the Ciliophora and the Radiolaria are not cells. They contain
more than one nucleus and therefore are syncytia. Other syncytia
are found in the Flagellata (Calonympha, Giardia), Rhizopoda
(Sappinia, Plasmodiophora), Sporozoa (Myxobolus) and Ciliophora
(Paramecium).
The advantage of deriving the metazoan from a syncytial
protozoan instead of a multicellular one is that in a syncytium such
as Calonympha or Opalina the animal has an already established
symmetry and an antero-posterior axis. All it has to do is super-
impose cell walls on the established pattern. In the development
of the multicellular form from the colonial pattern one has a series
of units each with an already established axis and these axes have
to be amalgamated and altered till the cells form a single unit.
This view of the syncytial origin of the Metazoa is supported
by de Beer (1954), who writes, " there are the gravest objections
to the view that the Metazoa were evolved by aggregation of
separate protozoan individuals. This may have happened in the
sponges and, indeed, is the most likely explanation for the lack of
co-ordination, integration and individuality found in those
animals. One of the most important features in the acquisition of
individuality in organisms is axiation and integration throughout
the body. The only way in which this can be imagined as having
occurred in the transition from Protozoa to Metazoa is by means
of internal subdivision of the protozoan cell, by cellularisation.
Nor is it difficult to imagine how this might have been brought
about, since there are Protozoa such as the Ciliate Infusoria,
Haplozoa and some Sporozoa which possess many nuclei, and it
would only be necessary to separate these by cell walls in order to
obtain the required organisation for the primitive Metazoa."
One difficulty comes when we consider whether the syncytium
has any inner cell walls or not. Thus if it can have cell walls
which do not divide the parts completely, then animals such as
Volvox which has connexions between the adjacent cells are
syncytia (Fig. 10). It is true that it is possible to consider that
Volvox has arisen by the accumulation of Chlamydomonas like
ORIGIN OF THE METAZOA 47
individuals whilst it is not possible to find any sub-unit for
Opali?ia. Nevertheless the differences between syncytia and
colonies are not as clear cut as has sometimes been supposed.
Another difficulty arises when we consider the stage during the
life cycle during which the protozoan is syncytial or colonial.
Thus many of the Protozoa form spores during reproduction and
these may be localised in spore cases. Are these to be regarded as a
multicellular stage? If so, then the palmella stage of Chlamy-
domonas could be a colonial form (Fig. 8). The Cnidosporidia
have many nuclei only during the reproductive (spore-forming)
stage; their trophozoite is unicellular and only has one nucleus.
Equally well the ciliate Anoplophrya, which does not separate
its asexually produced cells from the parent immediately they are
produced, can be considered as a colonial form (Fig. 14). In
effect the situation is quite difficult to resolve and depends to a
large extent on the relative duration of the multicellular stage and
the part that it plays in the life of the animal. Hadzi (1953)
has suggested that one of the major differences between the
Protozoa and the Metazoa is that the Protozoa have their major
phase in the reproductive stage whilst the Metazoa have their
major phase in the vegetative stage.
(3) Origin from the Metaphyta
The third view concerning the origin of the Metazoa is that
they arose from the plants, the Metaphyta. It has already been
mentioned that Franz (1926) thought that the Protozoa were in
fact derived from the Metaphyta and the Metazoa. Baker (1948)
suggested that the Metazoa arose from plant-like protozoans.
" The unicellular plant absorbs nutriment from all sides equally,
and when in the course of ontogeny or phylogeny it becomes a
metaphyte there is no fundamental change in this respect; a cell
divides without separation and the two products continue to
absorb nutriment over most of their surface. The passage from
unicellular form to the metaphyte is therefore easy. In the case of
animals, however, there is an important change when a unicellular
form becomes a metazoon; a new method of feeding must be
adopted. . . . The difficulties would be greatest when the pro-
tozoon had a localised mouth. If the products of such an animal
were to adhere together and each were to acquire its own mouth,
48 ORIGIN OF THE METAZOA
no advance could be made to the evolution of a metazoan alimen-
tary canal. This suggests that the Metazoa may have arisen
from primitive Protozoa unprovided with localised organs of
assimilation."
Hardy (1953), following on from Baker's argument, suggests
that " the Metazoa have not been derived from the Protozoa at all
but from relatively simple metaphytes, which after they had
evolved from the protophytes began, perhaps as a result of a
shortage of phosphates or nitrates, to capture and feed on small
organisms as do the higher insectivorous plants."
This is an interesting suggestion but one that can be criticised
on several grounds. There is no evidence that metaphytes such as
the Algae can withstand food shortages by catching animacules.
The thick cellulose cell wall around the metaphytes, though a
protection, would also tend to prevent them from developing
pse dopodia rapidly enough to catch protozoans. The insectivor-
ous plants, it will be remembered, all develop special insect-
catching mechanisms, and even so they still retain their photo-
synthetic ability.
Baker's arguments in favour of the origin of Metazoa from
plant-like protozoans can also be contested. There is no reason
why a metazoan type of alimentary canal should develop in the
first stages of the evolution of the Metazoa. The " alimentary
canal " of the sponges is not really comparable in function to that
of the higher metazoans, and even in the coelenterates there is a
considerable amount of amoeboid activity in the gut cavity. What
would appear to be more important than the development of an
alimentary canal is that the cells of the body should have some
continuity and interconnexion with each other so that food
material can be passed easily, from one cell to the other. Such a
process probably does occur in the colonial ciliates such as
Zoothamnion which have well-developed gullets. Summers (1938)
suggested that food material was probably passed along the stalk
of Zoothamnion. Here then we have the case of a protozoan with a
well-defined mouth forming a colony. Furthermore this colony
shows differentiation and division of labour, some of the polyps
being more intensive feeders than others.
There is no reason why a protozoan with a definite polarity
should not lose this polarity and develop into a colonial form.
ORIGIN OF THE METAZOA
49
Willmer (1956) in discussing the change of form of Naegleria
points out that the rhizopod can be in any one of three phases:
(1) in the flagellate stage with a definite polarity;
(2) in the amoeboid phase with pseudopodia coming from all
over the body ;
(3) aggregated in the form of a sheet of tissues.
It would seem that this protozoan has no difficulty in losing its
polarity and therefore that the difficulties raised by Baker con-
cerning the changes from Protozoa to Metazoa are not as great
as he suggests.
What conclusion then can be drawn concerning the possible
relationship between the Protozoa and the Metazoa? The only
thing that is certain is that at present we do not know this relation-
ship. Almost every possible (as well as many impossible) relation-
ship has been suggested, but the information available to us is
insufficient to allow us to come to any scientific conclusion regard-
ing the relationship. We can, if we like, believe that one or other
of the various theories is the more correct but we have no real
evidence.
CHAPTER 6
THE MOST PRIMITIVE METAZOA
We have seen so far that the Metazoa can be derived either from
syncytial protozoans, from multicellular protozoan colonies or
from the Protophyta. To some extent the theory that one chooses
as the most probable will depend upon which group is considered
to be the most primitive of the Metazoa. Thus if one considers the
Sponges as the most primitive of the Metazoa then one could
suggest a link between the Protozoa and the Metazoa via the
Choanoflagellata. If on the other hand one thinks that the
Acoelous Platyhelminthes are the most primitive metazoans, then
one could consider that the link with the Protozoa was via the
complex ciliates. It is therefore important to decide which are the
most primitive of the Metazoa, but before this can be done one
has to consider four questions.
(1) Which of the metazoan groups can be considered the
earliest to have evolved?
(2) Which are morphologically the most simple of the Metazoa?
(This will not necessarily be the first group to have evolved.)
(3) What is the relationship between the major groups of the
lower Metazoa?
(4) Can the Metazoa be considered as a polyphyletic group
with more than one origin from the simpler living forms?
The metazoans that will be considered here are the five groups :
(1) Porifera.
(2) Mesozoa.
(3) Coelenterata.
(4) Ctenophora.
(5) Platyhelminthes.
Before discussing these questions it will be as well to indicate
50
THE MOST PRIMITIVE METAZOA 51
the various uses of the expressions " primitive; simple; advanced;
radial symmetry and bilateral symmetry," since these terms will
frequently be used in the following discussion.
Primitive and simple
There are two terms that must be distinguished and used
carefully. The first term is " simple." If an animal has a
morphological structure made up from a few basic units, then such
an animal can be regarded as having a simple structure. Other
animals may have many different units arranged in a variety of
patterns ; they can then be regarded as having a complex structure.
These two groups, the simple and the complex, can also be
described as having a low level of complexity or a high level of
complexity.
The second term is " primitive." This means that of two
structures or conditions, one arose some time before the other. The
concept of "time of origin" is the critical point in determining
whether a structure is primitive or not. Because an animal has a
simple morphological pattern it does not mean that it had an
early evolutionary origin and therefore is in a primitive condition.
It is perhaps unfortunate that during most courses of Zoology
the students are taken from the Protozoa to the Primates and
shown the way in which the complexity of structure increases.
Quite often the student becomes puzzled when he deals with the
Mollusca. Should they come before the annelids, between the
annelids and the arthropods, or after the arthropods? It is clear
that this problem confuses two issues: firstly the complexity of
molluscs in relation to that of the annelids and the arthropods,
and secondly the time of origin of the molluscs, i.e. did they arise
before or after the annelids?
The student is usually taught that certain conditions can lead
to a simplification of morphological form and that clues other than
purely morphological ones must be used to elucidate an animal's
phylogenetic position. In particular this holds when we come to
deal with parasitic animals. Thus the larval form of Sacculina
quite clearly shows the crustacean ancestry of the parasite even
though the morphology of the adult is not at all typical of the
Crustacea. Though the parasitic habit is usually associated with
certain morphological changes, the other specialised ecological
5— IOE
52 THE MOST PRIMITIVE METAZOA
conditions are not often given equal credit for determining and
shaping an animal. Thus various morphological conditions will be
associated with a pelagic life, with burrowing, with living in sand,
with being a very large animal or being a very small animal. All
of these tend to alter the morphology of the animal and make it a
successful living animal, not just a representative of a hypothetical
idea; that of, say, a crustacean. An example of such an environ-
mental effect can be seen when we come to consider which is the
more primitive, radial symmetry or bilateral symmetry? (Fig. 17.)
Radial symmetry
This type of symmetry is often found in sessile or pelagic
animals. They usually have an oral and an aboral surface but
otherwise any diameter cut at right angles to the oral-aboral axis
should divide the animals into twro similar halves. In fact most of
the animals that are radially symmetrical do not fit in with this
definition since they usually have some irregularity in their
organisation, i.e. mesenteries, tentacles, madreporite, which allow
only certain sections at right angles to the oral— aboral axis to
divide the animal into equal halves.
Bilateral symmetry
The animals that show bilateral symmetry are organised into
an antero-posterior axis and a dorso-ventral axis. In addition there
is one plane and one plane only that will separate the animals into
equal right and left halves. A radially symmetrical animal will
have many such planes. Most of the Metazoa that are not pelagic
or sessile show a bilateral symmetry. (Fig. 17.)
One is often taught that the coelenterates and the echinoderms
show a basic radial symmetry and that the other Metazoa are
bilaterally symmetrical. Since the echinoderms and coelenterates
are sometimes placed at the foot of the metazoan evolutionary
tree it is not difficult to associate radial symmetry with a primitive
habit and to assume that the bilaterally symmetrical condition is
the more advanced. On the other hand, it is equally true that
radial symmetry is found in sessile or floating animals whilst
bilateral symmetry is found in crawling or swimming animals.
We are therefore left with the question, "To what extent does the
symmetry of an animal indicate its primitiveness and to what
extent does it reflect the habits of that animal? "
THE MOST PRIMITIVE METAZOA
53
(A). Radial Symmetry
(B). Biradial Symmetry
(C). Bilateral Symmetry
Fig. 17. Types of symmetry.
54 THE MOST PRIMITIVE METAZOA
There are certain exceptions to the generalisation that sessile
animals are radially symmetrical. Thus, as previously mentioned,
even amongst the coelenterates there are many planes that will not
divide the animal into two equal halves, this being due to the
development of tentacles, gonads, batteries of nematocysts,
mesenteries and siphonoglyphs. In other Metazoa it is rare to find
radial symmetry. Thus in the Rotifera, neither Trochosphaera
nor Melicerta are perfectly radially symmetrical. In the Annelida
Sabella is not radially symmetrical; its parapodia still show a
bilateral symmetry. In the barnacles, though there is some
tendency towards a radial symmetry as illustrated by the skeletal
plates, the internal symmetry of other organs such as the legs,
digestive system and nervous system is a bilateral one. Other
sessile animals such as the Crinoids, Ascidians and Pterobranchi-
ates do not show perfect radial symmetry. On the other hand the
ctenophores that take up a crawling habit such as Coeloplana and
Ctenoplana do show a very interesting bilateral (biradial) symmetry.
These examples indicate that subject to certain basic limita-
tions, the life that an animal leads will influence its shape and
basic symmetry. The question, " Is radial symmetry more
primitive than bilateral symmetry? " should perhaps be more
correctly replaced by the question, " Is the sessile or pelagic habit
more primitive than the swimming and crawling habit? " The
answer to the latter question is at present unknown.
(1) The Sponges (Porifera)
The sponges are peculiar multicellular animals with an organisa-
tion quite different from that of the other Metazoa. They have a
skeletal system and three layers of cells, pinacocytes, amoebocytes
and choanocytes, but they have no organ systems such as an
excretory or a nervous system. They have a very simple digestive
system in which there is no real mouth or gut. The sea water
around the animal passes through a series of apertures into the
centre of the sponge and in doing so is filtered, the food being
taken up by the choanocytes and the amoebocytes.
The organisation of the sponge is very simple in that a sponge
can be passed through the meshei of a net and so separated into its
individual cells. These cells can later aggregate and form an
organised sponge with the cells in their correct relative position;
THE MOST PRIMITIVE METAZOA 55
the mechanism of this interesting rearrangement is not yet under-
stood. This type of cellular organisation is found in the higher
Metazoa where it has superimposed on it the co-ordinating
influence of a nervous and hormonic integration, both of which
are apparently absent in the sponges. The high degree of skeletal
material relative to the small amount of living protoplasm makes
the sponges very poor food and so a relatively successful group of
animals.
Are the sponges a primitive or an advanced group of animals?
To answer this question we should have to know the time of
origin of the sponges and there is no certain information on this
point. Instead we can examine the apparently simple characters
and the apparently complex characters and attempt to derive some
satisfaction from this. The reader should always be on his guard
when consulting such lists ; it is not possible to come to a conclusion
merely by seeing which of the two lists is the longer !
Simple characteristics
(1) The layers of the body are loosely organised.
(2) The layers of the body do not correspond to the ectoderm,
mesoderm and endoderm of the higher forms.
(3) There is no definite body form.
(4) They have choanoflagellate cells like those present in the
choanoflagellate protozoans.
(5) There is no nervous system.
(6) There is no excretory system.
(7) There is no mouth.
(8) The gut (gastral cavity) shows little differentiation.
(9) They have a high regenerative capacity.
(10) They have a well-developed system of asexual reproduction.
(11) The larvae have well-developed flagella.
Complex characteristics
(1) They have three layers of cells (some coelenterates have only
two layers of cells).
(2) They have a well- developed middle layer, the " mesen-
chyme," with an elaborate skeletal system.
(3) They have some differentiation within the layers, e.g. the
pore cells.
56 THE MOST PRIMITIVE METAZOA
(4) They have a gut. (The Mesozoa have no gut.)
(5) The gemmules with which some sponges carry out asexual
reproduction are quite complex in structure.
(6) They have eggs and sperm.
(7) The embryo gastrulates in a complex manner, by ingression,
epiboly and delamination.
(8) They have a well-developed amphiblastula larva.
(9) The blastopore is aboral, in most other metazoans it is oral.
(10) An inversion of the layers occurs during embryology.
(11) The sponges are the only animals to have the main body
aperture the exhalant one.
Various excuses can be made for each and every one of the simple
or specialised characteristics. Thus, to deal with a few of them :
(1) Though it is correct that the layers are loosely organised this
may be due to the fact that the sponges do not depend on the
hydraulic pressure of the gastro-vascular cavity to maintain their
shape. They have a well-developed skeletal system that takes care
of this. The animal remains intact even though there are many
series of canals running through the body, and the cells are not
firmly cemented together.
(2) The layers do not correspond to the ectoderm, endoderm
and mesoderm of the higher animals and there is no evidence that
at one time they did correspond. There is not one piece of evidence
to show that the normal triploblastic condition evolved from that
shown by the sponges.
(3) Many sponges such as Euplectella and Poterion do have a
definite shape.
(4) Choanoflagellate-like cells are also found in the endoderm
of some coelenterates, annelids and molluscs. Electron microscope
studies show that the collar is a series of protoplasmic filaments
that project out of the cell in much the same way that the digestive
filaments project from an endodermal cell (Rasmont et al. 1958).
(5) There are other animals that have no nervous system, e.g.
the Mesozoa.
(6) The Mesozoa, Coelenterata, Ctenophora and Acoela have
no specialised excretory system.
(7) The gut in the sponges though it shows little differentiation is
at least a gut. There is no gut in the Mesozoa, Acoela or Pogonophora.
THE MOST PRIMITIVE METAZOA 57
(8) A high regenerative capacity does not indicate that an
animal is simple. Thus in the coelenterates, the polyps have good
regenerative capacity, the medusae do not. In the annelids the
Oligochaeta have good regenerative capacity, the Hirudinea do
not. In the amphibians the Urodeles regenerate well, the Anura
do not.
(9) There is no evidence that asexual reproduction is necessarily
more primitive than sexual reproduction.
It can be seen that the situation is not as straightforward as the
lists might at first sight make it appear. It should also be re-
membered that though one might believe that the sponges are
more simple than the coelenterates from the point of view of their
morphology and life cycles, this is no reason for thinking that they
necessarily developed some time before the coelenterates. The
sponges may have been a happy afterthought of the Protozoa
after they had given rise to the coelenterates !
Which group of animals did the sponges come from? There
are three different answers to this question. The first derives
the sponges from Protozoa such as the choanoflagellates or
Volvocinae. The second derives the sponges from a Gastrea type
of animal which gave rise to both the coelenterates and the
sponges. The gastrula probably came from a colonial protozoan
such as Volvox. The third answer derives the sponges from a
coelenterate source. Each of these views has something in its
favour and something against it.
Origin from the Protozoa
(i) From the Choanoflagellata
The inner layer of cells in the sponges is composed mainly of
Choanocytes. These in many ways resemble the cells of the
choanoflagellate protozoa and on this basis it has been suggested
that the sponges might be derived from these protozoans.
In 1880 Saville Kent described a colonial choanoflagellate
called Proterospongia (Fig. 18). This consisted of a flat plate of
about forty cells. The other cells had the normal choanoflagellate
structure whilst the inner cells were amoeboid. Periodically a
choanoflagellate cell would withdraw its flagellum and become
amoeboid, whilst an amoeboid cell would take up the position and
58
THE MOST PRIMITIVE METAZOA
(A). Proterospongia
(B). Sphaeroeca
Fig. 18. Colonial protozoa that in some ways resemble sponges.
(A) Proterospongia. (After Saville Kent.) This is now believed
to be a fragment of a fresh- water sponge.
(B) Sphaeroeca; single choanoflagellate protozoan and the colonial
form. (From Grasse after Lauterborn.)
THE MOST PRIMITIVE METAZOA 59
structure of a choanoflagellate cell. This protozoan had in many
ways the structure that one might expect to find in an ancestral
sponge and it has usually been figured as such in textbooks of
zoology.
Proterospongia is not a common protozoan. Recently Tuzet
(1945) has investigated the antecedents and morphology of this
protozoan and she decided that in fact Saville Kent was the only
person ever to have definitely seen Proterospongia and that what he
saw was not a protozoan but a small fragment of an actual sponge.
Tuzet concludes, " Pour nous. ... La Proterospongia de Saville
Kent n'est pas autre qu'un corps de restitution d'Eponge d'eau
douce." Proterospongia is nothing more than a restitution body
of a fresh- water sponge. If this is true it is not surprising that
Proterospongia has many sponge qualities. On the other hand
Grondtved (1956) has described a new species of Proterospongia,
P. dybsoensis, in which there are three to ten cells arranged in a
linear row per colony. These colonies were often found in very
large numbers, up to 2,300 colonies per litre of water, and
Grondtved thought that they might be fragments from a larger
colony except for the fact that they were all so much alike. There
does seem to be quite a considerable difference between the row of
three to ten choanoflagellate cells embedded in a gelatinous
common envelope and Proterospongia as described by Saville Kent,
where the choanoflagellate cells migrated into the interior of the
colony and took up amoeboid structure. For this reason it is not
clear whether the new species rightly can be placed in the genus
Proterospongia .
(2) From the Volvocinae
There are certain resemblances between the embryonic develop-
ment of Volvox and that of certain sponges. Duboscq and Tuzet
(1937) showed that in Grantia the embryo developed inside a
membrane. The blastula is made up of two types of cells,
flagellate ones and non-flagellate ones. In the blastula all the
flagellate cells point inwards at first but during the course of
development the blastula turns inside out so that the flagella now
point outwards. This phenomenon is called inversion and is
shown diagrammatically in Fig. 19. The larva is then liberated
as an amphiblastula larva with the flagella at one end. The other
60
THE MOST PRIMITIVE METAZOA
Fig. 19. Diagram to show inversion during the embryology of the
sponge Grantia. The embryo develops at first with its flagella
pointing inwards (1). The embryo slowly inverts (2-3) so that its
flagella now point outwards. (After Duboscq and Tuzet.)
end of the larva has the non-flagellated cells and after swimming
for some time the amphiblastula larva settles on the substratum,
the non-flagellated cells grow over the flagellated cells so that the
animal takes up the structure of an adult sponge.
A similar inversion takes place during the development of the
daughter colonies of Volvox (Pocock 1933). During the asexual
development of a daughter colony the daughter cells divide and
form a sheet of cells. These cells are orientated in the same manner
as the parent cells, the flagella pointing outwards, but as division
proceeds the daughter cells form a ball with the flagella pointing
towards the centre of the ball. The colony is not a complete
ball since there is a hole at the top. The colony now proceeds to
turn itself inside out through this hole in much the same way as
one might push a tennis ball inside out through a hole in the
wall (Fig. 20). This results in a colony with the flagella all
pointing outwards, the inversion taking some two hours.
THE MOST PRIMITIVE METAZOA
61
Fig. 20. Diagram to show inversion during the development of
daughter cells in Volvox. The flagella of the daughter colony all
point towards the inside of the colony. Inversion takes place and the
colony turns inside out so the flagella now point outwards. (After
Zimmerman.)
In both Volvox and Grantia the cells develop in the same initial
relationship to the embryo as they do to the parent layers. Hyman
(1940) was impressed by the similarity between the inversion in
Volvox and the sponges and suggested that this might indicate a
common ancestry. On the other hand Tuzet (1945) considered
the situation as one of convergence which does not indicate any
underlying phylogenetic relationship.
62 the most primitive metazoa
Origin from the Gastrula
This view holds that the sponges evolved from some form of
gastrula and was propounded mainly by Ernst Haeckel. Haeckel
from his studies of the embryology of the sponges (1872) decided
that the larval form of the sponge was a gastrula larva. He also
thought that certain other animals such as Haliphysema were
primitive sponges, though he later changed his mind.
Haeckel's views have had considerable influence on our current
zoological concepts. It was Haeckel who devised many of our
current words such as Phylum, Blastula, Morula, Gastrula,
Ontogeny, Phylogeny and many more. It is perhaps relevant that
we should spend a little time reporting how Haeckel developed his
ideas and concepts and the way in which these fitted in with
views on the origin of the sponges.
Haeckel spent many years developing his views on the phylogeny
of the animal kingdom. In effect he studied both the structure
and embryology of each of the various groups. Then by marrying
the facts and ideas from comparative anatomy and embryology,
Haeckel developed a sweeping plan of the relationship and evolu-
tion of various animal groups. He supported his schemes with
detailed arguments and when his opponents failed to understand
his arguments Haeckel devastated them with a barrage of crushing
sarcasm against their misinterpretation of his own specialised
terminology.
Simply stated, Haeckel's view was that the most primitive
animal was a small non-nucleated mass called the Monerula (Fig.
21). This was followed by a later group of animals that had a
nucleus and this state was called the Cytula. The Protozoa are
at the cytula stage. The next group of animals formed a solid
mass of nucleated cells called the Morula. The Morula led to a
more complex form that had a hollow centre and a single layer of
cells, the Blastula. Certain cells such as Volvox are almost at the
Blastula stage. The next stage in evolution was the Gastrula stage,
in which the animal had a double wall, a ciliated exterior and a
hollow gut.
The Gastrula assumed tremendous importance in Haeckel's
phylogenetic speculations. He thought that the Gastrula was the
ancestor of all the Metazoa, that it occurred in all the Metazoa at
THE MOST PRIMITIVE METAZOA
63
(o) Monerula
(b) Cytula
(c) Morula
(d) Blastuta
(e) Gostrula
Fig. 21. Haeckel's concept of levels of organisation. He suggested
that animals evolved through the successive adult stages shown in the
above figure.
some stage of their embryonic development and that a group of
animals existed which were adults but which were still at the
gastrula stage. Such animals were not known, but later Haeckel
thought he discovered such an adult group of animals and
he called them the Physemaria, an example of which was
Haliphysema.
Haliphysema, according to Haeckel, had the structure of a little
vase. The walls of this vase were made up of two layers of cells ;
the inner layer was flagellated, the cells having a collar-like
structure. The outer layer was made up from a syncytium of
cells. These outer cells took up stones and spines from the environ-
ment and covered the animal with a protective layer. They were
adults, since Haeckel described a series of gonadial cells which
were formed from the endoderm and then became liberated into
64
THE MOST PRIMITIVE METAZOA
the gut (Fig. 22). Many genera related to Haliphysema were dis-
covered and they all showed certain resemblances to sponges, i.e.
a central cavity lined with flagellated cells, and an outer layer of
cells covered by a skeleton which in this case differed from that
of a sponge in that it was not secreted but picked up from the
substratum. These animals assumed such tremendous importance
to Haeckel that at one time he derived all the Metazoa from the
Physemaria, but at a later date he decided that the Physemaria
were on a side line from the main Gastrula.
(b) Transverse section
(a) Longitudinal view
(c) Isolated choanoflagellate cell
Fig. 22. Haeckel's view of the structure of Haliphysema. He
thought that the structure was that of a simple sponge, (a) shows
the whole animal with part of the body cut away to demonstrate
the inner structure, (b) is a transverse section of Haliphysema and
shows the gonads migrating into the interior of the animal, (c) shows
in more detail the structure of the inner flagellate cells. It is
doubtful if such a detailed pattern exists in Haliphysema or if such a
simple condition exists in any sponge.
THE MOST PRIMITIVE METAZOA 65
A difference of opinion arose between Haeckel and other
workers over the structure of the Physemaria. Saville Kent in 1878
from studies of both living and fixed material decided that
Haliphysema was no sponge but instead a foraminiferan rather
like Euglypha. He was unable to see any of the internal details
described by Haeckel. A controversy soon arose between Haeckel
and Saville Kent and it was left to Ray Lankester, as a friend of
Haeckel, to enter the controversy in the role of adjudicator.
Lankester asked Saville Kent for specimens of Haliphysema
and then examined them both alive and in the fixed and stained
condition. After considerable examination Lankester (1879)
decided that Saville Kent was perfectly correct in his assertions
and that the specimens were clearly those of a foraminiferan. But
the matter did not end there. Lankester ingenuously decided that
the answer to such a controversy was extremely simple. He sug-
gested there must be two different genera of animals which from
the outside looked exactly alike but one of these had been studied
by Professor Haeckel whilst the other had been studied by Mr.
Saville Kent. Lankester had no doubt that the isomorph studied
by Haeckel would have the structures that Haeckel had described
and he hoped that Professor Haeckel would supply him with some
specimens. It does not appear that such specimens were ever
sent to Lankester.
Perhaps something should be said in Haeckel's defence. In a
recent paper on Haliphysema tumanowiczii, Hedley (1958) describes
the way in which the protozoan often picks up sponge spicules
and covers itself with these. Also certain individuals were
multinucleate, a condition which in certain circumstances might
be confused with some of the conditions described by Haeckel.
Haeckel continued to believe in the importance of the Physemaria
though he thought that the Gastrula was more important (1899).
He derived all the Metazoa from the Gastrula and stated, " I
regard the Gastrula as the most significant and important
embryonic form in the whole animal kingdom. It occurs amongst
the sponges, Acalephe, the Annelida, Echinodermata, Arthropoda,
Mollusca, and the Vertebrata as represented by Amphioxus. In
all these representatives of the most various animal stocks, from
the sponges to the vertebrates, I deduce, in accordance with the
Fundamental Biogenetic Law, a common descent of the whole
66 THE MOST PRIMITIVE METAZOA
animal world from a single unknown stock form, Gastrula or
Archigastrula, which was essentially like the gastrula." (Mono-
graph on Calcispongiae.)
These ideas were not accepted even in Haeckel's own time.
Thus both Claus and Schmitt disagreed with him, and as Radl
(1930) states, " The popular idea of the method of the scientist is
that he assembles a series of definite facts upon which he founds his
case. We see that this is not always the case. It is not true that the
facts which told against the Gastrula were unknown at the time
when the theory was propounded, or that the theory was gradually
discredited as the facts which contradicted it were gradually
accumulated until it finally had to be abandoned. Everything that
has ever been cited against the theory was known when the theory
was put forward; nevertheless it was widely accepted. Today
some still accept it, others do not." Though it is perhaps an over-
statement that " everything that has ever been cited against the
theory was known when the theory was put forward," Radl's
point is made quite clear. The theory was often accepted because
it was attractive and not because it was supported by detailed
verified factual information.
One may conclude, therefore, that there is at present no
evidence that the sponges arose from an adult gastrula. They have
neither a hollow gastrula larva nor are there any simple sponges
that are still in the gastrula condition during the adult stage. The
situation as Haeckel saw it was based on over-simplification and
misinterpretation of the evidence.
A modification of the Gastrula theory has recently been pro-
posed by Jagersten (1955). He suggested that the primitive
blastula gave up living and swimming in the sea and started to
crawl on the sea bottom (Fig. 23). It modified its structure to
become a " Bilateroblastea " with a flattened ventral surface, an
arched back, a few sensory cells at the front of the body and the
sexual cells inside the body. The centre of the body was hollow
and not filled with mesodermal cells. At first the animal fed
phagocytically all over the body surface, but as food particles
accumulated on the ventral surface the phagocytic ability became
restricted to the ventral region. This then became raised from the
ground till the animal took up the shape of the " Bilaterogastrea '
as shown in Fig. 23.
THE MOST PRIMITIVE METAZOA
67
(b)
Fig. 23. Bilaterogastrea theory. Jagersten has suggested that
the primitive larval form was that of a bilaterogastrea. The
planula larva (a) settled on the ground, raised its ventral surface
to accommodate food material (b, c) and so developed a gut (d, e,
f). It then takes up the form of a Bilaterogastrea. (From
Jagersten.)
Jagersten's scheme is derived from his view that the primitive
form had a hollow centre and was not filled with mesenchyme.
The reason he thinks that the primitive form had a hollow interior
is that otherwise the various groups of animals such as the
coelenterates, platyhelminthes, etc., would have had to develop a
hollow gut independently and on several different occasions.
Secondly, though he agrees with the statements that the endoderm
6— IOE
68
THE MOST PRIMITIVE METAZOA
in the Hydrozoa is formed by the wandering in of cells, in the
Scyphozoa, Anthozoa and higher animals the endoderm is often
formed by invagination. Since on other grounds Jagersten thinks
that the Anthozoa are more primitive than the Hydrozoa, he
suggests that invagination is the more primitive system in the
formation of endoderm and that the primitive larva had a hollow
centre, i.e. a gut, and was not solid as has been suggested by
Hyman (1940).
The following system is therefore suggested by Jagersten to
explain the development of the Porifera from the bilaterogastrea.
The bilaterogastrea settled on the sea floor and placed the
middle of its elongated mouth on the substratum. The water and
food material flowed in through the mouth and out via the anus.
The mouth later became folded and developed a series of pores as
shown in Fig. 24. The anus remained a single structure and
migrated to a dorsal position to become the exhalant opening. The
animal then had the form of a sponge though it would still have
to develop the peculiar histological structure of the Porifera.
J agersten's view is of interest in showing what could have happened.
Whether the Porifera did actually arise in this manner is open to
doubt.
Fig. 24. Jagersten's view of the evolution of the sponges. The
bilaterogastrea settled on the bottom (a), raised its mouth from
the substratum (b) and then divided the mouth into many oscula
(c). The anus then migrated dorsally (f, g). (e) is a transverse
longitudinal section of a.
the most primitive metazoa 69
Origin from the Coelenterata
This view, that the coelenterates and the Porifera have close
ancestral affinities is quite an old one. It is based on the fact that
the coelenterates and the sponges often have a solid planula-type
larva during their embryology. Lankester (1890) strongly sup-
ported this view when he emphasised the differences between the
planula larva and the Gastrula. He thought that there was no
indication that the sponges ever had a gastrula stage but that
instead the resemblance was in the solid blastula.
In Leucosolenia the fertilised egg divides to form a sixteen-
celled hollow blastula. The majority of the cells are flagellated but
a few at one end are non-flagellated. These non-flagellated cells
together with a few of the flagellated cells migrate into the interior
of the blastula and fill the central cavity. The result is a solid
blastula. This settles on the ground, flattens and the inner cells
then migrate out on top of the flagellated cells. They then become
the pinacocytes and amoebocytes, whilst the flattened flagellated
cells turn into the choanocytes.
Though there are certain similarities between the development
of the sponges and the coelenterates, it is difficult to know how
much reliance can be placed on them. Thus Balfour (1880) was
quite clear that there was no relationship between the cell layers
of the sponges and those of the coelenterates since the inner layers
of the sponge embryos come to lie on the outside of the adult.
For the same reason Delage (1898) suggested that the sponges have
their endoderm on the outside and the ectoderm on the inside and
that the sponges should be called the " Enantiozoa " for this
reason. It is of interest that Saville Kent (1880) described the
way in which the outer cells of the sponge, the pinacocytes, could
take in food particles.
It is possible to enumerate the similarities and differences
between the sponges and the coelenterates as follows.
Similarities between sponges and coelenterates
(1) They are both aquatic and free-living animal groups.
(2) They have spicules in their skeleton, which are either
calcareous or horny.
(3) They have flagella.
70 THE MOST PRIMITIVE METAZOA
(4) Amoebocytes are present in both groups.
(5) The main body cavity is neither a haemocoel nor a coelom.
(6) There are no excretory organs.
(7) They occasionally have mesenchyme but never mesoderm.
(8) They form buds or gemmules for asexual reproduction.
(9) They have sexual reproduction with sperm and eggs.
(10) They both form colonies.
(11) They both have a high regenerative capacity.
(12) They have a solid blastula larva (stereoblastula) before the
amphiblastula or planula larva develops.
(13) The anterior end of the larva becomes attached to the
ground.
(14) The sex cells are formed by interstitial cells or amoebocytes.
Differences between sponges and coelenterates
(1) The sponges have many entrances to the body cavity.
(2) The main body opening of the sponges is the exhalant one.
(3) The sponges have choanocytes (but see p. 56).
(4) The outer layer of the sponge is never ciliated in the adult.
(5) There are no nematocysts in sponges.
(6) The sponges have no muscles or musculo-epithelial cells
(except porocytes).
(7) The sponges have no nervous system or sense organs.
(8) The sponges do not show polymorphism.
(9) The sponge spermatozoa are sometimes carried to the egg by
amoebocytes.
(10) The sponges never form a compact skeleton such as is seen
in certain coelenterates such as the corals.
(11) The adult sponges are never pelagic.
(12) There is no clear homology between the layers of the
sponges and the layers of the coelenterates.
Though the above lists do not actually prove anything they
do indicate that the differences between the coelenterates and the
sponges are quite considerable and basic. It is thus doubtful if
there is any close relationship between these two groups. It is
also impossible to state whether the sponges arose earlier than the
coelenterates. Their organisation is less complex in some ways,
but this again does not necessarily mean that the sponges are
THE MOST PRIMITIVE METAZOA
71
therefore more primitive than the coelenterates. Our conclusion,
therefore, is that the situation is not at all clear.
(2) The Mesozoa
The Mesozoa are a group of parasitic animals of very simple
structure. They are multicellular and usually take the form of a
solid mass of cells with one or more internal cells. These internal
cells are not digestive in function but instead play a part in the
reproduction of the animal.
The mesozoans in some ways correspond in structure to a solid
blastula and it has been suggested by some writers such as van
Beneden (1876) and Hyman (1940) that the Mesozoa are a
primitive group, or even the most primitive group, of the Metazoa.
On the other hand the Mesozoa are all internal parasites. Thus
(a) Ciliated larva
(b) Female
(c) Male
Fig. 25. Mesozoan structure. Rhopalura.
(a) Ciliated larva. (From Hyman after Atkins.)
(b) Adult female. (From Hyman after Caullery.)
(c) Adult male. (From Hyman after Caullery.)
72
THE MOST PRIMITIVE METAZOA
one group, the Dicyemida, represented by Dicyema, is found in the
kidney of the Octopus, whilst the other group, the Orthonectidae,
represented by Rhopalura, is found inside various marine inverte-
brates. Both these groups have a ciliated larva which may bore
into a new host and this larva in some ways resembles the
miracidium larva of the digenetic trematodes (Figs. 25 and 27).
The Mesozoa also have a complex life cycle, and this together with
the larval structure has led writers such as Stunkard (1954) and
Caullery (1951) to think that the Mesozoa are probably digenetic
trematodes. The recent Traite de Zoologie edited by Grasse also
places the Mesozoa amongst the platyhelminthes. We thus have
two views concerning the Mesozoa; one that they are primitive
animals, the other that they are degenerate parasites.
-INVERTEBRATE HOST-
Plosmodium >-Agannete-
Male
Female
•Ciliated larva-*-
- Zygote
Fig. 26. Diagram of the life cycle of Rhopalura. (After Caullery.)
It should be stated at the very beginning of this discussion that
the Mesozoa have suffered as a group in that various non-related
animals such as Haplozoon have been thrust into the Mesozoa
though in fact their affinities are elsewhere (see p. 41). There is
also some doubt about the closeness of the relationship between the
Orthonectids and the Dicyemids. The resemblance lies in their
simple morphology and the fact that both have a ciliated larva,
but since they are both internal parasites, the simple morphology
is suspect straight away. One knows that other internal parasites
such as the males of Bonelia, or the parasitic cirripedes, become
very simplified. On the other hand the adult trematodes and
cestodes are not morphologically simple — there being a tremendous
development of the reproductive systems.
Dodson (1956) has suggested that though a parasitic life can lead
to morphological simplifications in the parasite, it does not
THE MOST PRIMITIVE METAZOA
73
(a) Infusoriform
larva
(b) Older larva
Fig. 27. Mesozoan structure. Dicyema.
(a) From Hyman after Nouvel.
(b) From Hyman after Lameere.
(c) From Hyman.
©
mz
4 •
':.©.
»&
(c) Nematogen
necessarily do so. Thus animals such as the leech are parasitic
but complex in structure, and, as we have already mentioned,
many of the platyhelminthes and nematodes are quite complex.
When one also considers the fact that the mesozoans have a
complex life cycle, some stages of which are not yet known, it
would appear premature to place the mesozoans in a key position
between the Protozoa and the Metazoa.
It is possible to draw up lists of the simple characters and the
platyhelminth-like characters of the Mesozoa. These are as
follows.
Simple characters of the Mesozoa (non-platyhelminth
characters)
(1) They are multicellular animals with no differentiation into
endoderm, ectoderm or mesoderm.
74 THE MOST PRIMITIVE METAZOA
(2) They have a solid blastula.
(3) There is a simple adult form; there are no proglottides,
no suckers, no thick cuticle, no nervous system, no flame
cells, no complex gonadial system.
(4) They have cilia and a few reproductive cells as their
specialisations.
(5) The cilia of the trematode miracidium larva are soon lost ;
those of the Mesozoa last throughout the life of the animal
(not in the Orthonectids).
(6) There is no cell in the miracidium comparable to the
internal nematogen cells of the adult Dicyemids.
Resemblances between the Mesozoa and the digenetic
trematodes
(1) They are internal parasites.
(2) They have a complex life cycle.
(3) Both the trematodes and the Mesozoa show polyembryony.
(4) The trematode miracidium larva and the Orthonectid
ciliated larva have the following similarities.
(a) The larva results from similar unequal cleavage of the
fertilised ovum.
(b) The larva is bilaterally symmetrical.
(c) The larva has a fixed number of cells.
(d) The larva is ciliated.
(e) The larva does not feed.
(/) On arrival in the host, the somatic cells degenerate
and the generative cells develop.
(g) The larva is the distributive phase between one host
and the next.
(5) The adult male Orthonectid has a reproductive duct.
Details of the structure and life history of the Mesozoa are given
in Figs. 25-28. Our knowledge of the life cycle of the Ortho-
nectids is fairly complete but that of the Dicyemids is not. Thus
we do not know if they have a second host, and, if so, the
morphology of the parasite in this host. A suggested life cycle is
shown in Fig. 28 and this cycle is more complex than that
described for the Orthonectids (McConnaughey 1951).
THE MOST PRIMITIVE METAZOA
OCTOPUS-
75
Rhombogen
1
occasional
^. Secondary
Nematogen
Stem Nematogen
???+
Infusorigen
[Infusorifo"m larva]
Fig. 28. Diagram of the life cycle of Dicyema. (After
A IcConnaughey.)
Caullery (1951) stated that it was probable that the adult of
Orthonectids such as Rhopalura would on future examination
show greater histological differentiation. ' A more careful
histological analysis than so far made will probably disclose a
nerve ring. What is lacking is a digestive apparatus, as in the
Monstrillidae, and here this is almost certainly because the life
of the adult is here even more ephemeral, and entirely devoted to
the production and dissemination of larvae." Caullery is clearly
of the opinion that the Orthonectids are degenerate forms.
There is no certainty that the Orthonectids and the Dicyemids
are as closely related as their grouping together in the Mesozoa
suggests. The resemblances are mainly that both have a ciliated
larva and the adult structure is multicellular without a gut or
organ systems. The life cycle of Dicyema is not yet fully known
and so it is difficult to compare it with Rhopalura. There is a
plasmodial stage in Rhopalura which has not been described for
Dicyema. The ciliated larva is not identical in structure in the two
forms.
If the Mesozoa are not primitive, they can be considered as
degenerate digenetic trematodes, possibly the miracidium larva
of some trematode that has become the end stage of development,
e.g. the Mesozoa are neotenous miracidia. There are, as we have
seen, certain resemblances between the miracidium and the ciliated
76 THE MOST PRIMITIVE METAZOA
mesozoan larva, but as yet no miracidium has been described which
is as simple as the mesozoan larva. The mesozoan larva has a very
short life and so it might not have time to develop the flame cells
found in the miracidium. Perhaps some experimental studies on
miracidia and the condition under which they can be maintained
will allow us to come to a greater understanding of the Mesozoa.
There is also a great deal to be discovered about the life history and
habits of this group of animals before we can come to any con-
clusion about their phylogenetic position.
(3) The Coelenterata
Over the early years there was a controversy over the animal
nature of the Coelenterata and it took some time before their true
animal nature was recognised (Johnstone 1838). Even so, various
groups of animals such as the Ectoprocta, Endoprocta and the
Coelenterata were grouped together mainly on the similarities of
their external form.
T. H. Huxley in 1849 presented a memoir on the anatomy and
affinities of the Medusae to the Royal Society of London. In this
memoir he described how the Medusae differed from the rest of the
animal kingdom in that they could be regarded as having only two
layers whilst the other metazoans had three layers. Huxley sug-
gested that the layers in the Coelenterata were homologous with
those of the Vertebrata and that in fact the Coelenterata were
diploblastic.
In Huxley's text A Manual of the Anatomy of the Inzertebrated
Animals published in 1891 he modified his views a little. He
classified the coelenterates into two main groups, the Hydrozoa
and the Actinozoa, and he included the Medusae in the Hvdrozoa.
(1) Hydrozoa: (a) Hydrophora Tubularia.
(b) Discophora Aurelia.
(c) Siphonophora Physalia.
(2) Actinozoa: (a) Coralligena Actinia.
(b) Ctenophora Pleurobrachia.
He compared the coelenterate body to a sac. " The walls of the
sac are composed of two cellular membranes, the outer of which is
termed the ectoderm, and the inner the endoderm, the former
THE MOST PRIMITIVE METAZOA 77
having the morphological value of the epidermis of the higher
animals, and the latter that of the epithelium of the alimentary
canal. Between these two layers, a third layer — the mesoderm —
which represents the structures which lie between the epidermis
and the epithelium in more complex animals, may be developed,
and sometimes attains great thickness, but it is a secondary and,
in the lower Hydrozoa, inconspicuous production. Notwithstand-
ing the extreme variety of form exhibited by the Hydrozoa and the
multiplicity and complexity of the organs which some of them
possess, they never lose the traces of this primitive simplicity of
organisation and it is but rarely that it is even disguised to any
considerable extent. ... In the fundamental composition of the
body of an ectoderm and an endoderm, with a more or less largely
developed mesoderm, and the abundance of thread cells, the
Actinozoa agree with the Hydrozoa There is a certain similarity
between the adult state of the lower animals and the embryonic
conditions of the higher organisations. For it is well known that,
in a very early state, even of the highest animals, it is a more or less
complete sac, whose thin wall is divisible into two membranes,
an inner and an outer. . . . There is a very real and genuine
analogy between the adult Hydrozoon and the embryonic vertebrate
animal, but I need hardly say it by no means justifies the assump-
tion that the Hydrozoa are in any sense ' arrested developments '
of higher organisms."
From the above account by Huxley two points are clear. Firstly
he thought that the resemblance between the embryonic develop-
ment of the higher animals and the organisation of the coelenter-
ates into two main layers of importance as indicating the primitive-
ness of the coelenterates. Secondly Huxley realised that mesoderm,
or its precursor, did occur in the coelenterates and thought that
there was an increase in the thickness and complexity of the
mesoderm in the higher coelenterates. In effect he assumed that
simple Hydrozoa such as Hydra and Tubularia were more
primitive than the members of the Actinozoa.
There are now two questions that should be considered. The
first is what are the simple and complex characters of the
coelenterates? From a study of these it should be possible to
assess how near the coelenterates are to the basic metazoans. The
second problem concerns the relationship of the Hydrozoa,
78 THE MOST PRIMITIVE METAZOA
Scyphozoa and the Actinozoa, and in effect revolves around which
of these can be considered as being the most primitive. As we
have seen, Huxley considered that the Hydrozoa were the more
primitive, but many zoologists now think that the Actinozoa are
the more primitive.
Let us now consider the simple and the complex characters of
the coelenterates. Some of these, as shown in the following lists,
are contradictory, but this is due to the wide range of structure
occurring within the coelenterates.
Simple coelenterate characteristics
(1) There are only two well-developed epithelial layers,
ectoderm and endoderm.
(2) They have a mesogloea.
(3) They have musculo-epithelial cells.
(4) The ectoderm may be ciliated.
(5) The gut has only one opening.
(6) There is a hydraulic skeleton.
(7) They are free living forms and not parasitic.
(8) Digestion is both intra- and extra-cellular.
(9) There is no respiratory or excretory system.
(10) They are polymorphic.
(11) They have a high regenerative capacity.
(12) They have a planula larva.
(13) The nerve net shows little concentration.
(14) They show radial symmetry.
Complex coelenterate characteristics
(1) They may develop cells in the mesogloea to form mesen-
chyme and mesoderm.
(2) The body layers may become quite complex, e.g. three types
of cells in the ectoderm: (a) sensory and mucus cells; (b)
interstitial cells; (c) muscle cells.
(3) They may have separate muscle cells (Trachylina and
Scyphozoa) which may be striated. The musculature can
be complex, e.g. circular, longitudinal and oblique muscle
bands.
(4) They develop a skeletal system. This may be an exoskeleton
in Obelia or Heliopora or an endoskeleton as in Cor allium.
THE MOST PRIMITIVE METAZOA 79
(5) They have a gut. (The Mesozoa and Acoela have no gut.)
(6) The gut may have subdivisions (pharynx, mesenteries).
(7) The gut develops a circulation in Aurelia and Alcyonium.
(8) They have nematocysts.
(9) They have specialised sense organs such as eyes and
statocysts.
(10) Some coelenterates are bilaterally symmetrical.
(11) Some coelenterates such as Velella and Porpita show
division of labour.
As is well known, there is considerable diversity of structure
within the coelenterates, and even though various coelenterates
can be derived from a common plan there is still difficulty in
deciding which are the most primitive coelenterates as opposed to
the most simple. Thus though one can arrange a series going
from, say, Hydra to Physalia, or from a diploblastic radially
symmetrical form to one that is triploblastic and bilaterally
symmetrical, there is no historical justification for either such
series. We must find some collateral evidence to help determine
which are the most primitive of the coelenterates.
The most primitive coelenterates
There is hardly a group of the coelenterates that has not at one
time or another been claimed to have been the most primitive.
Perhaps the two most prevalent claims are (1) that the polyp is
the most primitive form, and (2) that the medusa is the most
primitive form.
The view that the polyp is the most primitive form in the
coelenterates has been supported by Haeckel, de Beer and Hadzi
as well as various other writers. Whilst Haeckel suggests that
Hydra is primitive, Hadzi thinks that the anemones are more
primitive and that evolution within the coelenterates has gone
from the Anthozoa to the Scyphozoa and Hydrozoa. This view
is supported by de Beer (1954), who writes, " It follows and is
generally recognised, that the polypoid person which is the only
one represented in the Anthozoa, is more primitive than the
medusoid person found in the Scyphozoa and Hydromedusae,
which is clearly an adaptation to dispersal on the part of the sessile
form."
80 THE MOST PRIMITIVE METAZOA
It is interesting to compare the above statement with one taken
from Hyman (1940). " The contrary theory, that the ancestral
coelenterate was a primitive medusa, therefore seems more
acceptable. This could readily have developed from the meta-
gastraea by putting forth tentacles and wThen armed for food
capture would not have been limited to a bottom habitat." R. C.
Moore (1956) is of a similar opinion to Hyman. " Next the
conclusion that the polypoid and medusoid types of organisation,
instead of representing a more or less unexplained ' alternation of
generations ' constitute the products of evolutionary differentia-
tion in which the polypoid form is a persistent early growth, and
the medusoid is the normal adult type of coelenterate, leads to the
interpretation of medusoids as the initial type of coelenterate. This
is consistent with the paleontological record, which includes
numerous Lower Cambrian and even Precambrian medusoid
fossils. Consequently the simplicity of the hydroid forms is not
accepted as a basis for placing them in first position among
various types of coelenterates. Precedence is assigned to early
medusoids."
Though the medusa has been suggested as the basic form in the
Coelenterata this has not been followed up by claiming that the
Scyphozoa are the most primitive class of the Coelenterata. The
life cycle of the Scyphozoa with their dominant medusa and their
temporary polyp (hydratuba) might fit in with the primitive system.
The Stauromedusae such as Haliclystus and Lucernaria indicate
the way in which an adult polyp, even a highly specialised polyp,
could have arisen. The nematocysts in the Scyphozoa are more
limited in range of form than those in the Hydrozoa. It might
be objected that the medusae of the Scyphozoa are very much
more complex than those of the Hydrozoans, but the complexity
of the present-day forms does not mean that the original forms were
of the same complexity. The present-day forms and even the
Cambrian fossils have a tremendous history of development
behind them. The choice of a primitive class in the coelenterates
will clearly depend upon the light that such a choice throws on our
understanding of coelenterate morphology.
The most popular choice of primitive class in the coelenterates
seems to lie between the Hydrozoa and the Anthozoa. Opinion is
divided as to which of the Hydrozoa are the most primitive. Thus
THE MOST PRIMITIVE METAZOA 81
a selection of authors and their choice of primitive form is shown
below.
Haeckel Hydrida
Moser Siphonophora
Hyman Trachylina
It is difficult to choose between the above groups; thus though
Hydra is more simple in its adult morphology, it is suggested
from a study of the range of form that the medusoid condition is
more primitive in the Hydrozoa and that development from this
led to the solitary polyp.
On the other hand there is a growing body of opinion that the
Anthozoa are more primitive than the Hydrozoa. This view is
supported by Hadzi (1944), Ulrich (1950), Remane (1955),
Jagersten (1955) and Marcus (1958), who suggest the develop-
mental sequence went Anthozoa-Scyphozoa-Hydrozoa. No
closely reasoned account has yet been presented by the above
authors to show exactly how the morphology of the primitive
anthozoan would lead one to suppose that they are more primitive
than the hydrozoans, but the gist of the evidence is apparently as
follows.
(1) If the Hydrozoa were the most primitive forms which later
gave rise to the Anthozoa this would not explain the marked
bilateral symmetry found in the Anthozoa. Bilateral symmetry is
usually associated with a mobile habit and one would not expect to
find it in a sessile form that had a long sessile history behind it.
This bilateral symmetry is found in the Ordovician Tetracorallia
and even in the arrangement of nagella in the zooxanthella larva.
From the symmetry as shown in the arrangement of the mesenter-
ies, the retractor muscles, septal filaments, siphonoglyphs and
sulcus, one would suppose that the Anthozoa arose from a free-
living mobile ancestor.
(2) A second reason for choosing the Anthozoa as the most
primitive form lies in the range and structure of the nematocysts.
The Hydrozoa have over a dozen different types of nematocysts
whilst the Anthozoa have only about half a dozen different types.
Furthermore the cnidoblast that carries the nematocysts is more
simple in the Anthozoa; it lacks the cnidocil and instead has a
primitive ciliary cone (Pantin 1942).
82 THE MOST PRIMITIVE METAZOA
(3) The Anthozoa, Scyphozoa and many of the higher animals
form their endoderm by invagination. This method is rarely
found in the Hydrozoa, where ingression is more usual, and this
latter situation has been regarded as being a specialised condition.
If we accept these reasons for choosing the Anthozoa as the
primitive class of the coelenterates, what would the primitive
form look like? It might have been something between an
Antipatharian and a Protanthean. In the Antipatharia there are
only six, ten or twelve septa. The longitudinal musculature on the
septa is scanty or absent and the flagellated tracts are very simple.
The mesogloea is scanty and the siphonoglyph only weakly
developed. In Protanthea there are eight macrosepta and four
microsepta. There is a complete cylinder of longitudinal epidermal
muscles in the column and pharynx (these are much reduced in
other Anthozoa). The nerve net and ganglion cells are well
developed over the surface of the body — the ectodermal nerve net
being reduced in other anemones. The sphincter and basilar
muscles are absent. The retractor muscles are weakly developed
and there are neither septal filaments nor a siphonoglyph.
Although forms such as Antipathes or Protanthea may be simple
Anthozoa, they are still very complex when compared to a
protozoan. We still know very little about the primitive anthozoans
but it requires a lot of imagination to bridge the gap between the
Antipatharia and the Protozoa.
Are the Coelenterata the most primitive of the lower
Metazoa? We have to choose between the Mesozoa, Porifera,
Coelenterata, Ctenophora and the Turbellaria to find the most
primitive metazoan. It seems likely that the simplicity of the
Mesozoa can be discounted as due to their entirely parasitic
nature. Similarly the sponges can be discounted since their level
of organisation is quite different in nature from that present in the
other metazoan. It would be best to place the sponges on a side
line to the main line of origin of the Metazoa ; the time of origin
of the side line is not clear.
There is no doubt that the simplest of the Hydrozoa are more
simple than either the Ctenophora or the Turbellaria. But as we
have already mentioned, we do not know that simple forms such as
Hydra are the most primitive of the Coelenterata. One of the
major clues that has been used to place the coelenterates has
THE MOST PRIMITIVE METAZOA 83
been that of embryological development. Haeckel suggested that
the adult coelenterates such as Hydra were at a stage comparable
to the gastrula seen in Ampkioxus. Even in Haeckel' s time it was
pointed out that the embryology of the coelenterates did not
follow that of the higher animal. The blastula of the Hydrozoa
is most often a solid larva, the interior of which is filled with
cells. Hadzi and de Beer take this solid larva to indicate that the
primitive larva had a solid gut and they think that the coelenterates
cannot be primitive since they have a hollow gut. It may be
correct that the most common type of planula has a solid
interior. But this in no way indicates that the adult also had a
solid gut.
The Acoela are not the only animals to have a solid gut in the
adult condition. Within recent years the Pogonophora, a group
related to the Pterobranchiate Protochordates, have been
described by Ivanov (1954-7). They have a solid gut filled with
endoderm cells. The Pogonophora are coelomate animals and it
is not clear whether the solid gut is here a primitive condition or
one that is due to the small size of the animal. At any rate it leads
one to wonder about the precise conditions that lead to the
retention of the solid gut if it is a primitive condition, or the
development of a solid gut if it is an advanced condition. Jagersten
(1955) thinks it highly unlikely that the primitive metazoans had a
solid gut since this would mean that the hollow gut arose at least
twice, once in the Coelenterata and again in the Turbellaria. It is
perhaps worth noting that certain coelenterates such as Clytia,
when they feed, fill the gastro-vascular cavity with endodermal
processes so that the gut takes on a solid mesh-like appearance.
Thus Hadzi's view that the Coelenterata cannot be the most
primitive of the Metazoa since they have not a solid gut is open to
two objections: firstly we do not know that the solid gut is a
primitive condition and secondly some coelenterates can at times
show a condition resembling a solid gut.
In conclusion, then, it is apparent that we do not know whether
the coelenterates are more or less primitive than other lower
metazoans such as the Turbellaria. We do not know if the hollow
gut is a primitive condition. We do not know if the Hydrozoa are
more primitive than the Anthozoa. WTe do not know which is the
more primitive form, the medusa or the polyp, and as we shall
7— IOE
84 THE MOST PRIMITIVE METAZOA
now see, we do not know the relationship between the Coelenterata
and the Ctenophora.
(4) The Ctenophora
There are three questions that should be discussed concerning
the Ctenophora. (1) What is their ancestry? (2) Are they
coelenterates? (3) Are they ancestral Turbellaria? These are all
difficult questions to answer and involve a careful consideration of
the structure of the ctenophores.
The ancestry of the Ctenophora
Nothing definite is known about the ancestry of the ctenophores.
It is generally suggested that they arose from a basic stock that
gave rise to the coelenterates; thus there are certain resemblances
and certain differences between the ctenophores and the coelenter-
ates, as can be seen from the lists below.
Coe
(1
enterate characteristics of the Ctenophora
There are two primary layers ; the ectoderm and endoderm
are well developed and there is no definite mesoderm — just a
mesenchyme.
The main body cavity is the gastro-vascular cavity.
There is only one opening to the gut — the mouth. There is
no true anus.
They have a stomodeum at the entrance to the gut as in the
anemones and some medusae.
The gut is divided like that of the Scyphozoa but the eight
divisions are more like the symmetry of the Alcyonaria.
They are radially symmetrical.
They have mesenchyme muscles like some of the coelenter-
ates, e.g. Trachylina, Scyphozoa.
The gonads are derived from interstitial cells.
The outer surface has cilia ; as comb plates in Pleurobrachia,
as a ciliated surface in Coeloplana.
The tentacles are like those of some Scyphozoa.
The lasso cells may take the place of nematocysts, but
Euchlora has true nematocysts.
There are no nephridia.
They have a subepidermal nerve net.
THE MOST PRIMITIVE METAZOA 85
(14) Gastrodes has a planula larva.
(15) Certain coelenterates such as Hydroctena resemble
ctenophores.
Differences between Coelenterata and Ctenophora
(1) Some ctenophores have openings to the gut other than the
mouth. (Similar openings are found in some medusae such
as Aequorea.)
(2) The lasso cells are morphologically quite distinct from
nematocysts. The nematocysts of Enchlora have been
stated to have been derived from its food.
(3) There are no musculo-epithelial cells.
(4) Coeloplana and Ctenoplana have genital ducts.
(5) The cilia are arranged in specific rows, or comb plates
(except for Coeloplana).
(6) Their symmetry is more biradial than radial.
(7) The embryology of the ctenophores is determinate and the
cleavage differs markedly from that of the coelenterates.
Can the Ctenophora be placed in the Coelenterata? It can
be seen that there are many resemblances between the coelenter-
ates and the ctenophores. The two greatest differences seem to lie
in the possession of nematocysts by the coelenterates and the
embryology of the two groups. The ctenophores do possess lasso
cells which differ in their morphology from the nematocysts found
in the coelenterates. However, one ctenophore, Euchlora rubra,
has been found to have nematocysts. When these were investi-
gated by Komai (1942) he found that the nematocysts occurred
in the tentacles and inside cells which he thought were endodermal
cells. In 1951 Komai suggested that the nematocysts might have
been taken from the food of Euchlora since the nematocysts did not
lie on the surface of the tentacle but were sunk into the ectoderm.
Hadzi (1951) thought that the nematocysts in Euchlora were
derived from its food, there being a close resemblance between its
nematocysts and those of the narcomedusan Cunina.
Picard (1955) reinvestigated this problem and found that the
nematocysts did in fact lie on the surface of the ectoderm, correctly
orientated for discharge. The nematocysts were only found in
association with ectodermal cells, never endodermal cells. Picard
86
THE MOST PRIMITIVE METAZOA
Fig. 29. Ctenophora. A typical ctenophoran such as Pleurobrachia
shown here is a round transparent animal with eight ciliated comb
rows. (From Hyman.)
suggested that the nematocysts were formed mainly during the
larval phase of the ctenophore. The nematocysts differ in
structure from those of the narcomedusae, which would indicate
that they cannot be derived from Cunina. Furthermore all the
specimens had nematocysts.
All these points lead one to conclude that Euchlora has its own
true nematocysts. This would then indicate that the ctenophores,
or at least this ctenophoran, belong to the Cnidaria !
The apparent wide embryological differences between the
coelenterates and the ctenophores may be diminished when we
know more about the range of embryological development of the
THE MOST PRIMITIVE METAZOA 87
Scyphozoa. For the ctenophores in many ways resemble the
scyphozoans; thus, both have a poor regenerative ability in the
adult, they both develop thick mesenchyme and they both
develop muscles. Considerable interest was aroused by the dis-
covery of the medusa Hydroctena. Haeckel suggested that it was
an ancestral form to the Ctenophora and it certainly shows a
superficial resemblance to a ctenophore as can be seen from Fig. 31.
The resemblances are due to the ovoid shape, the two tentacles
(which Haeckel thought could be retracted into pockets at their
base) and the gut being divided into four pockets. On the other
hand there are many differences. Hydroctena has a circular canal
around the perimeter of its body, the tentacles are oral and non-
retractile (those of the ctenophores are aboral and retractile).
There is no statocyst, it has nematocysts and not lasso cells, and
the gonads develop on the wall of the manubrium instead of the
radial canals. What is of interest here is the manner in which the
ctenophoran form can be imitated by a medusoid form.
Another interesting coelenterate that shows certain ctenophore-
turbellarian affinities is Tetraplatia. It was classified as a nar-
comedusan hydrozoan by Carlgren (1926) placed in a separate
order of the Hydrozoa, the Pteromedusae by Hand (1955), but
identified as a coronate scyphozoan by Krumbach (1927). Its
external form is elongate and very much like that of a Muller's
larva. There are eight lappets around the body, this giving some
resemblance to a ctenophore; on the other hand the mouth is
terminal (Fig. 31). Tetraplatia' s affinities are further discussed by
Ralph (1959).
It is unfortunate that the planula larva is not more common in
the ctenophores. The only known case is in Gastrodes, which is
parasitic on Salpa. Otherwise the ctenophores have a typical
cydippe larva. There are some clear affinities between the
coelenterates and the ctenophores but just how closely the two are
related is hard to say. If further investigations show the presence
of nematocysts to be more widespread than just in Euchlora and
if they are of a similar pattern to the coelenterate nematocysts and
not like those of the protozoan nematocysts, it will indicate that
the ctenophores can be included in the Cnidaria. The relationship
between the Hydrozoa, Scyphozoa and Anthozoa seems to be a
closer one than that of these three to the Ctenophora.
88
THE MOST PRIMITIVE METAZOA
(A). Ctenoplana (dorsal view)
(After Komai.)
(B). Ctenoplana (side view)
(After DawydofT.)
(C). Coeloplana (dorsal view)
(After Komai.)
Fig. 30. Aberrant ctenophores. These ctenophores take up a
crawling habit and their shape differs from that of Pleurobrachia.
THE MOST PRIMITIVE METAZOA
89
Tetraplatia Hydroctena
Fig. 31. Aberrant coelenterates.
Tetraplatia shows superficial resemblance to the Miiller's larva of
the polyclad platyhelminthes. (After Krumbach.)
Hydroctena. This medusoid form shows certain resemblances to
a ctenophore. (After Dawydoff.)
Relationship of the Ctenophora to the Turbellaria
Although typical ctenophorans such as Plenrobrachia or
Hormiphora are round pelagic animals there are some creeping
forms. It was these creeping forms and in particular Coeloplana
(Fig. 30) that led Lang (1884) to suggest that the ctenophores gave
rise to the polyclad Turbellaria. It is not hard to bridge the
gap between the pelagic forms such as Pleurobrachia and creeping
forms like Coeloplana. Thus Lampetia is a semi-globular form that
sometimes crawls on its everted pharynx. Ctenoplana in its
swimming form is clearly a ctenophore (Fig. 30B) but in its
crawling form it spreads itself out on its oral lobe and becomes a
flat animal. Finally Coeloplana is a flattened form like a turbellarian
(Komai 1922) and it looks very much like a link between the
ctenophores and the polyclad Turbellaria. In transverse section
Coeloplana has a complex structure (Fig. 33) and it is not sur-
prising that Lang thought that it was the forerunner of the
turbellarians. In particular he associated it with the polyclads
because of the many branches of the gut. The polyclad resem-
blances can be seen from the following list.
90 THE MOST PRIMITIVE METAZOA
Resemblances between Coeloplana and the Polycladida
(1) Both have a flat, compressed body.
(2) They move by creeping on the sole of the " foot."
(3) The body surface is ciliated.
(4) There is a well- developed basement membrane.
(5) The dermal musculature is well developed; the dorso-
ventral muscles may be branched.
(6) The gastric canals have many branches; there is no anus
but some pores end externally.
(7) There is a stomodeal invagination on the ventral surface.
(8) Both show determinate cleavage.
(9) The large micromeres give rise to small micromeres.
(10) The micromeres form the ectoderm.
(11) There is no hollow blastula stage.
(12) The development is mosaic.
(13) The mesoderm arises from the macromeres.
(14) The embryo gastrulates by epiboly.
(15) The Muller larva present in some polyclads has eight
ciliated lappets.
(16) There is a small apical nervous tuft.
(17) There is a statolith.
(18) Both groups have paired tentacles.
(19) There are gonadial canals.
The above list is impressive in length and indicates a consider-
able similarity between the two groups. Lang suggested that the
centrally positioned nerve centre in the ctenophores moved
anteriorly to take up the typical polyclad position, i.e. a change
from biradial symmetry to bilateral symmetry (Fig. 32). The list
may also demonstrate another point. Often in discussing such a
problem, a list of characters is drawn up of the points for and the
points against a given viewpoint. The difficulty comes when one
has to decide the relative importance of each character. It is
impossible to come to a decision just by seeing whether there are,
say, more similarities than differences. Instead each point must be
weighted according to its importance and this is difficult since the
importance often reflects the opinion of the observer.
In spite of the similarities between Coeloplana and the Poly-
cladida, the general opinion these days is that the similarities are
THE MOST PRIMITIVE METAZOA
91
(A). Ctenophoran condition
(B). Hypothetical condition
(C). Polyclad condition
Fig. 32. Lang's concept of the manner in which the ctenophores
could have given rise to the polyclads. The anus moved ventrally
and backwards and the body form became elongated.
92
THE MOST PRIMITIVE METAZOA
due to convergence and that Coeloplana and Ctenoplana are in fact
specialised aberrant and advanced forms. In particular there are
considerable differences between the embryology of the cteno-
phores and the polyclads which make it improbable that the two
groups are related. These differences are not due to the presence
or absence of yolk but instead reflect a more fundamental differ-
ence. The ctenophore egg cleaves into four and at the next
cleavage it divides to form a small group of cells, the micromeres,
and a large central group, the macromeres. These form a flat
plate of cells. Cleavage continues till there are eight macromeres
and many micromeres. In the polyclads, on the other hand, after
the four-cell stage the embryo shows a definite spiral cleavage
pattern. The cells can all be classified in terms of the spiral cleavage
pattern found in the Rhabdocoelida, Tricladida, Annelida and
Mollusca. This spiral cleavage is not found, nor is there any
indication of spiral cleavage, in the development of the
Ctenophora.
There are other differences between the polyclads and the
ctenophorans. Thus the polyclads have a well-developed brain,
mesenchyme
lumen of
food canal
muscle fibre —
eosinophil_
body
° O o
1 Q.°0J. o o ,o
• o o ° • -P • » ° °„
° O • n r, °"o ° n° °»°
gland cell-- -£-
ciliated
epidermis
Fig. 33. Diagrammatic transverse section through the body of a
ctenophore, Coeloplana. (After Komai.)
THE MOST PRIMITIVE METAZOA
93
often the most highly developed brain of all the turbellarians ;
they also have well-developed and numerous eyes, flame cells,
a complex reproductive system with a muscular penis, uterus,
seminal vesicle and prostate organ, and often show hypodermic
impregnation. The Ctenophora have nothing to compare with
this.
It is interesting to mention here that Hadzi (1944) and de Beer
(1954) think that the Ctenophora arose from the Polycladida, a
viewed discussed in more detail on page 94. Hadzi places the
Ctenophora in the platyhelminthes though he agrees that
Coeloplana and Ctenoplana are aberrant forms.
What conclusion can we come to regarding the position of the
Ctenophora? With regard to their level of organisation they are
in most respects at a similar level to that seen in the Anthozoa-
Scyphozoa line of the Coelenterata. It is not possible to place
them any closer than this until more research has been carried out
on the embryology and development of the ctenophores and until
the range of form of the coelenterates is better known. It is not
' 1 j.lll L ! J J-l? -1.'.'. J J.U^ jJJJLL'-lLU-'-'-lJjj J-t JJji J JiJJJ JJJJ.J.1. 1 LLJAl i ! U-'.'.'IV. ciliated epithelium
glandular cell
mesenchyme
food vacuole
— muscle fibre
rr~ — "~
pharynx
Fig. 34. Diagrammatic transverse section through the body of an
Acoelan, Convoluta. There is a certain resemblance to the grade
of organisation of the ctenophorans. (After von Graff.)
94 THE MOST PRIMITIVE METAZOA
even certain at this stage that the ctenophores and coelenterates
had a common origin. It is possible that the nematocysts of the
ctenophores could have arisen independently of those in the
coelenterates ; after all there are some well-developed nematocysts
in the Protozoa. On the other hand there is almost nothing to
favour the view that the ctenophores are platyhelminthes. This is
particularly so because the turbellarians have a well- developed
reproductive system with accessory muscular sacs, whilst the most
that any ctenophore has is a small reproductive duct. There is
thus no clear indication that the ctenophores either gave rise to
or were derived from the Turbellaria.
(5) The Platyhelminthes
Though the platyhelminthes are usually considered as having
evolved after the Coelenterata, Hadzi (1944, 1953) has suggested
that this is not the case and that in fact the coelenterates evolved
after and from the platyhelminthes. The classification that Hadzi
gives of the lower Metazoa is as follows.
Phylum
Subphylum
Class
Spongiaria
Spongiaea
Ameria
(1) Platyhelminthes
Planuloidea
Turbellaria
Ctenophora
Trematoda
Cestoda
(2) Cnidaria
Anthozoa
Scyphozoa
Hydrozoa
This classification differs from the usual one in several respects.
First of all the platyhelminthes are considered to be the most
primitive of all the Ameria, more primitive than the Cnidaria.
Secondly the Ctenophora are placed in the platyhelminthes.
Thirdly the Anthozoa are considered to be the most primitive of
the Cnidaria. The evolutionary sequence devised by Hadzi is as
follows.
THE MOST PRIMITIVE METAZOA
95
Hydrozoa
t
Anthozoa
t \
Ciliata — > Acoela -> Rhabdocoelida Scyphozoa
\ .
Polycladida — > Ctenophora
Hadzi thinks that the Metazoa arose by the formation of cell
walls in a syncytial ciliate. This would then lead to a multicellular
animal with a complete organisation, i.e. an antero-posterior axis
and without the difficulties of reorganisation that a multicellular
brain
glandular
secretion
.statocyst
0"
p&,
:'Lfood vacuole
mesenchyme
Ff^:':7. v.-.SM::- ift- '.•':'•• ':, --mouth
• ■ ■■ •'• & ••':..•. • ••• :•",.. • ■A.I
food-5
vacuole
oenis
ovary
bursa
seminalis
___ Reproductive
opening
cilia
Fig. 35. Diagrammatic longitudinal section through an Acoelan
to show the order of complexity of its structure. Note the
development of a complex reproductive system. (From Bronn.)
96 THE MOST PRIMITIVE METAZOA
colonial animal might have had. The syncytial level of organisa-
tion would correspond to the solid blastula, the stereoblastula,
that is sometimes found in the embryology of the Metazoa. The
simplest Metazoa did not have a hollow gut and corresponded in
structure to the present-day Acoela (Fig. 35).
The Acoela gave rise to the other platyhelminthes, amongst
which were the Rhabdocoelida with their straight gut, and the
Polycladida with their branched gut. The Rhabdocoelida gave
rise to the Anthozoa which in their turn gave rise to the Hydrozoa
and the Scyphozoa. The Polycladida have a swimming larval
form, the Miiller's larva, and this became neotenous and gave
rise to the Ctenophora. Neotenous Miiller's larvae have been
described; thus Heath (1928) described Grafizoon lobata which
resembled a sexually mature Miiller's larva.
The arguments that Hadzi puts forward in favour of his views
are as follows and he is supported by de Beer (1954, 1958).
The Coelenterata are not primitive
(1) The radial symmetry shown by the coelenterates is second-
arily acquired by them. The development of bilateral symmetry is
shown first of all in the external parts of the higher animals and is
then impressed on the internal organs. In the coelenterates such
as the Anthozoa, the bilateral symmetry is only found internally
as in the mesenteries. Therefore it must have lost its external
bilateral symmetry and be in the process of acquiring a radial
symmetry concomitant with a sessile habit.
(2) The polyp is more primitive than the medusoid form.
Since the polyp is found in the Anthozoa whilst the Hydrozoa have
both polyp and medusa it follows that the Anthozoa are the most
primitive of the Coelenterata.
(3) The Coelenterata are not diploblastic. They have a well-
developed middle layer, the mesogloea, which often contains
cells. Furthermore the cell lavers in the Anthozoa and the
j
Hydrozoa are not strictly comparable since in the Hydrozoa the
germ cells are formed from the ectoderm whilst in the Anthozoa
and the Scyphozoa they are formed from the endoderm. The
germ layers in the coelenterates are not comparable to the germ
layers of the higher animal and are not even homologous within
the coelenterates.
THE MOST PRIMITIVE METAZOA 97
(4) Haeckel suggested that the Coelenterata represented the
hollow gastrula stage found in the embryology of the Echinoderms,
Sagitta and Amphioxus. This would indicate that the coelenterates
are a primitive group. But we now know that the blastula is more
often a solid form and that the endoderm is not always formed by
the invagination and development of a hollow gut. In fact the
hollow gut is an advanced condition when compared with that
present in the Acoela.
Objections can be raised to all of Hadzi's points.
(1) There is no evidence that the radial symmetry is secondarily
acquired by the coelenterates. The detection of an external
symmetry depends upon having some external organs; the
coelenterates do not have any such organs along the length of the
polyp and thus they cannot display this external bilateral sym-
metry. It cannot therefore be established that they had an
external bilateral symmetry at some stage which was later lost.
Furthermore there is no evidence that bilateral symmetry is
acquired first of all by the external organs and later by the internal
organs.
(2) It is not generally accepted that the polyp is the most
primitive form in the coelenterates. In fact there is quite a
body of opinion that holds the medusa to be the primitive form
(see p. 80).
(3) Though it is correct that not all the coelenterates are
diploblastic, the mesogloea of many of the Hydrozoa shows little
or no development. They at least can be considered as having an
effective diploblastic condition. As for homologising the cell
layers, it is not strictly correct to assert that the gonads arise
from the ectoderm in the Hydrozoa. It is more correct to state
that they arise from interstitial cells. In this way, therefore, one
can homologise the germ layers within the coelenterates.
(4) Finally the fact that the blastula may often be solid in no
way indicates that the adult must have had a solid gut in
the most primitive metazoans. The larval form merely indicates
what the primitive larval condition was like, not the adult
condition.
Having asserted the non-primitive nature of the coelenterates
Hadzi presents the following evidence that the Acoela are more
primitive than the coelenterates.
98 THE MOST PRIMITIVE METAZOA
The Acoela are primitive
(1) The Acoela organisation corresponds to that of a ciliate
that has developed cell walls.
(2) The Acoela have no gut.
(3) The Acoela are hermaphrodite and have internal fertilisa-
tion rather like the syngamy of the ciliates.
(4) The Acoela often have a syncytial gonad, epidermis, repro-
ductive system and digestive system. This is a relic of the
original ciliate syncytium.
(5) The digestive system of the Acoela can be derived from the
protozoan food vacuoles (Figs. 5 and 35).
(6) The nephridial system can be derived from the protozoan
contractile vacuoles. The Acoela do not have flame cells.
(7) The Acoela usually have a ciliated ectoderm.
(8) The Acoela often have musculo-epithelial cells.
(9) The Acoela have no basement membrane.
(10) The Acoela have a central mouth like the ciliates.
(11) The Acoela have a simple pharynx derived from a
stomodeum.
(12) There are no distinct gonads.
(13) The rhabdites are derived from the trichocysts.
The Acoela and the Polycladida differ in their morphology and
development from the rest of the Turbellaria. Hadzi suggests that
the Acoela gave rise to the Rhabdocoelida and the Polycladida.
The Rhabdocoelida then gave rise to the Anthozoa by the loss of
their protonephridia, the reduction of their nervous system, the
simplification of their digestive system, the loss of accessory
reproductive organs and reduction of the mesoderm. The slime
glands of the epidermis of the rhabdocoels gave rise to the
nematocysts.
The derivation of the Anthozoa from the Rhabdocoelida in this
way would be very surprising with no other parallel in the animal
kingdom, i.e. reduction and simplification giving rise to a whole
phylum of widely diverse and successful animals. This does not
mean that such a reduction is impossible; it just seems highly
improbable. It also seems unlikely that the polyclads gave rise to
the ctenophores.
THE MOST PRIMITIVE METAZOA 99
There is also little assurance that the Acoela are the most
primitive of the Turbellaria. They are a comparatively unstudied
group of animals; we know next to nothing about their physiology,
little experimental embryology has been performed on them and
we do not know their range of morphological forms. Though von
Graff (1904) was of the opinion that their structure was primitive,
a great deal more research will have to be carried out before such a
position can be justified and even more research will be necessary
before they can seriously be derived from the ciliates. For
further details concerning the phylogeny of the platyhelminthes
and their relationship to the Ctenophora one should consult
Bresslau (1933).
There is a school of thought represented by Marcus (1958) which
suggests that the platyhelminthes are an advanced group of
animals that were once coelomate and more complex morphologic-
ally than, say, the Nermertini, Phoronidea or Brachiopoda. The
platyhelminthes according to this view are secondarily simplified.
They have lost their coelom, anus and circulatory system. They
have reduced their nervous system, and altered their reproductive
system to make up for the loss of the coelom. It is suggested that
one well-known example of a coelom being lost when an animal
takes up parasitic habit is that of the Hirudinea, and that the
platyhelminthes have gone even farther along this course.
We thus have two conflicting views concerning the status of the
platyhelminthes. Hadzi suggests that they are the most primitive
of all the Metazoa, being more primitive than the coelenterates
and derived from the ciliates. Marcus suggests that the platyhel-
minthes are an advanced group of animals whose simplicity of
structure is due to their parasitic habit and that they arose some
time after the Nemertea.
What can one conclude about the most primitive of the Metazoa?
There are, as we have seen, five contestants, Porifera, Mesozoa,
Coelenterata, Ctenophora and the Platyhelminthia, for this title.
These groups are almost completely isolated from each other
though a few tenuous connexions can be made. It is quite clear
that the available evidence is insufficient to allow us to come to
any satisfactory conclusion regarding their interrelationships. At
the same time it is also clear that a great deal of work remains to
be done on all of these groups. We are still very ignorant about the
8— IOE
100 THE MOST PRIMITIVE METAZOA
comparative physiology and biochemistry of the lower Metazoa
and very little experimental work has been done on their
embryology. It is possible that these lines of research will help
in the elucidation of the relationships between the lower Metazoa.
It is also possible that the new information will indicate more
clearly that the Metazoa are polyphyletic.
CHAPTER 7
THE INVERTEBRATE PHYLA
Within the invertebrates there are many distinct phyla. So far
we have considered some of the possible relationships between the
so-called " lower phyla," namely the Protozoa, Porifera, Mesozoa,
Coelenterata, Ctenophora and Platyhelminthia. There are, how-
ever, many other important phyla such as the Nematoda, Nemertea,
Rotifera, Annelida, Arthropoda, Mollusca, Brachiopoda, Echino-
dermata and Protochordata that all deserve some mention for they
each present special problems of phylogenetic relationship.
It is not possible to obtain satisfactory palaeontological data
concerning the relationship of these various phyla because most
of them are already fully established in the earliest fossil-bearing
beds, the Cambrian. This means that one has to use other inform-
ation to determine the relationships between these phyla. In
fact these relationships are not at all clear and this can best be
illustrated by examining three attempts that have been made to
present a coherent monophyletic relationship of the major
invertebrate phyla.
Grobben's Classification
Karl Grobben in 190S proposed a scheme to show the inter-
relationship of various invertebrate groups. This system has
formed the basis for most of our current schemes, e.g. Cuenot
1952. The system divides the major invertebrate phyla into two
sections, the Protostomia and the Deuterostomia. This distinction
had been proposed by Goette in 1902 and was based on the fate
of the blastopore in the developing embryo: whether it becomes
the anus or the mouth and anus. In the Protostomia the blastopore
becomes the mouth and anus whilst in the Deuterostomia it
101
102 THE INVERTEBRATE PHYLA
becomes the anus; the mouth develops in another position.
Grobben then divided the phyla in the following fashion.
Protostomia Deuterostomia
Scolecida Chaetognatha
Molluscoidea Echinodermata
Mollusca Enteropneusta
Annelida Tunicata
Arthropoda Acrania
Vertebrata
By Scolecida, Grobben meant the Platyhelminthia, Entoprocta,
Aschelminthia and Nemertini. In the term Molluscoidea he
included the Phoronidea, Ectoprocta and Brachiopoda. Sometimes
the group Molluscoidea was referred to as the Tentaculata.
Let us first of all consider the validity of these two major groups,
the Protostomia and the Deuterostomia. In the Protostomia the
situation is not as clear cut as the classification might suggest.
Thus in the platyhelminthes, the blastopore closes in Convoluta
and Planocera and the mouth is a new formation (there is of
course no anus in the platyhelminthes). In the polyclads the
original blastopore closes and disappears but the pharynx develops
near the site of the erstwhile blastopore. In the Tardigrada the
blastopore does not develop. In the Entoprocta the blastopore
closes and a new mouth and anus develop. In the Annelida the
situation varies according to the animal studied. In Nereis and
Podarke the blastopore forms the mouth and anus in the required
manner. In Pomatoceros the blastopore forms the mouth but the
anus is a new formation. In Capitella, Ctenodrilus and Saccocirrus
the blastopore closes and the mouth and anus are new formations.
In the oligochaete Dendrobaena the anus is a new formation and it
is not derived from the blastopore.
In the Arthropoda the situation is much the same. In Peripatus
capensis the blastopore after a brief closure opens again to form
the mouth and anus. In some crustaceans such as Caridina the
anus develops some distance away from the blastopore region
whilst the mouth develops as a new formation unrelated to the
blastopore. In Astacus the proctodeum arises from the region near
the site of the blastopore.
THE INVERTEBRATE PHYLA 103
In the Mollusca the fate of the blastopore also varies. In the
Gastropoda as a rule the anterior part of the blastopore gives rise
to the mouth, in Paludina the mouth arises from the posterior
part of the blastopore. In all gastropods the anus is a new
formation unrelated to the blastopore. In the Amphineuran
Ischnochiton, too, the anus is a new formation. The lamellibranches
such as Teredo or Cyclas have the blastopore closed completely
and the mouth and anus are entirely new formations. Otherwise
the blastopore becomes the site of the mouth. Further informa-
tion can be found in DawydorT (1928) and Manton (1948).
In the Deuterostomia the fate of the blastopore is similarly
varied. The echinoderm mouth is a new formation in the larva
whilst the blastopore becomes the larval anus. The same is true
for the hemichordates. In the Tunicata and the Cephalochordata
the blastopore becomes dorsally placed to form the neuropore. In
the Chaetognatha the blastopore closes and does not become
either the mouth or the anus.
It can be seen that the division into Protostomia and Deuteros-
tomia is not as sharp as might be expected. Thus certain groups
such as the Tardigrada, Chaetognatha, Tunicata, Cephalochordata
and so on would be in neither the Protostomia nor the Deuteros-
tomia. In other groups such as the Annelida or Arthropoda,
certain genera have the blastopore forming the mouth whilst
others do not.
This situation was appreciated quite early. Thus Sedgwick
stated in 1915, " In Peripatus the mouth and anus are not only
derived from the elongated blastopore by its constriction into two
openings but remain throughout life included within the nerve
ring derived from the neural rudiments of the embryo. If in
other Arthropoda, in Annelida, and in the Mollusca we find, as
we do, that the nerve ring referred to is, in the adult, incomplete
behind the anus, and the mouth and anus, though obviously
referable to the blastopore, are not actually derived from it, must
we on this account deny this most obvious relation and maintain
that the mouth or anus, as the case may be, in these forms is not
homologous with that of Peripatus} To maintain such a position
appears to us impossible and we entirely accept the doctrine that
the mouth and anus of the Annelida, Arthropoda, and Mollusca
are both perforations of the embryonic neural surface and are
104 THE INVERTEBRATE PHYLA
Tunicata Arthropoda
Acrania / Chaetognatha Echinodermala
Vertebrata
Enteropneusta
Mollusca
Annelida
(Chordonia) ^omalo- (Ambulocralia)
pterygia)
Spongiaria
Molluscoidea
(Deuterostomia)
Ctenophora
(Coelenterata)
Metazoa
Rhizopoda
Sporozoa
Ciliata
(Cytoidea)
Flagellata
(Cytomorpha)
Protozoa
Fig. 36. Grobben's classification of the Invertebrate Phyla.
specialisations of parts of one original opening which is repre-
sented in most embryos by the blastopore.
" When, however, we come to apply this doctrine to the Chordata
we stand on more debatable ground. Placing the Enteropneusta
on one side as not obviously conforming to our plan, we find that
it is a fact of observation that in the Chordata the blastopore
THE INVERTEBRATE PHYLA 105
perforates the embryonic rudiment and that in some of them the
anus is directly derived from it. (Many Pisces, some Amphibia,
e.g. Newt.) Whereas in others not at all remote from these, the
blastopore closes entirely and the anus is a new formation (some
Pisces and Amphibia, e.g. Frog, Amniota). Here also we think
it may be fairly maintained that notwithstanding the diversity in
the mode of development of the anus, it is, in all vertebrata at
least, a derivative of the blastopore."
It will be seen from Sedgwick's account that whilst he realised
there was considerable diversity in the fate of the blastopore, he
thought the generalisation — that the blastopore became the
mouth in the Protostomia and the anus in the Deuterostomia — a
fair one. On the other hand Manton (1948) thinks that the
variability in the mode of development of the mouth and anus is so
great in the Annelida and the Arthropoda that it no longer forms a
useful link between these two groups. " It is clear that most of the
known species of Onychophora fall into line with the Arthropoda
in the dissociation of the mouth and anus from the blastoporal
area and contrast with the majority of the Polychaeta."
There are other characters that can be used to separate the
Protostomia and the Deuterostomia, or the Annelid and the
Echinoderm Superphylum as they are sometimes called.
Annelid Superphylum Echinoderm Superphylum
Spiral cleavage Radial cleavage
Blastopore = mouth Blastopore = anus
Schizocoelic coelom Enterocoelic coelom
Determinate cleavage Indeterminate cleavage
Nervous system delaminates Nervous system invaginates
Ectodermal skeleton Mesodermal skeleton
Trochosphere larva Pluteus type larva
To each and every one of these characters many exceptions
can be found and in particular, certain groups of animals seem to
lie between the two superphyla. Thus the Brachiopoda have their
blastopore forming the mouth, their coelom is enterocoelic and
their cleavage is of the radial type. The situation is most difficult
for the Nematoda, Ectoprocta and Phorodinea and these are the
groups that one would most like to place accurately. Even within
106 THE INVERTEBRATE PHYLA
the major groups there is some disagreement. Thus Raven in his
account of morphogenesis in the Mollusca states that it is incorrect
that the group as a whole shows determinate cleavage. This would
indicate that the Mollusca-Annelida link is not necessarily as
close as some authors imagine. On the other hand it is necessary
to keep some sense of balance and not lose sight of the wood
because of the trees.
Grobben's classification is shown in Fig. 36. In some ways it
resembles the next classification to be discussed, that of Marcus,
but there are certain differences. Thus the Coelomata arise from
the line that led to the Ctenophora. The Enteropneusta are more
allied to the Echinodermata than they are to the Tunicata or
Vertebrata.
Marcus's Classification
This view of the phylogeny of the invertebrates has been
described by Marcus (1958) and it agrees in many ways with that
described by Grobben and also with that described by Ulrich
(1950) and Remane (1954). Marcus considers that the Anthozoa
are the most primitive of the Coelenterata. All the forms above
the Coelenterata are called " Bilateria " since they are almost all
bilaterally symmetrical. They are also called " Coelomata " and
Marcus considers that all these forms are derived from an
ancestor that had the " fundamental features of the Archicoelomata,
viz. three coeloms, mouth, anus, vessels and perhaps tentacles."
The coelom was developed as a series of pouches from the gut, as
suggested by Sedgwick (1884), and the Bilateria could have arisen
from either the Anthozoa or the Ctenophora.
Since the Bilateria are all coelomate this means that the
Platyhelminthia, Rotifera, Nematoda and Endoprocta all are
derived from a form that once had a coelom. During the course
of evolution the coelom became reduced in these forms till some-
times all that is left is the cavity of the flame cells. The resemblance
that has been reported between the planula larva and the Acoela,
Marcus suggests, is entirely due to the small size of the animals.
The Bilateria are divided by Marcus into the Protostomia and
Deuterostomia, as we have already seen in Grobben's classification,
the only addition being the newly described Pogonophora, which
are placed in the Deuterostomia. Marcus points out that there
THE INVERTEBRATE PHYLA
107
are certain real resemblances between the animals at the base of
the Protostomia and the base of the Deuterostomia. Thus the
Ectoprocta and the Pterobranchiata have a body that is in three
segments; the Ectoprocta and Brachiopoda are enterocoelic, the
Ectoprocta have coelomic pores and budding is often similar in
pattern.
The first major division within the Protostomia is the Tenta-
culata, which is comparable to the Molluscoidea of Grobben.
Of these the Phoronidea are considered as being the most primitive
whilst the Entoprocta are considered to be derived from attached
larvae of the Ectoprocta.
The Nemertea are coelomate, their coelom being restricted to
the rhynchocoel and the gonad cavities. The nemerteans are more
primitive than the Turbellaria since they have an anus and their
Aschelminthes
f Arthropodo I
V. v J
^Annelida A,0||usca
Platyhelminthes
Nemertini
Fig. 37. Marcus's classification of the Invertebrate Phyla.
108 THE INVERTEBRATE PHYLA
genitalia are more simple. Their embryology indicates a possible
relationship with the polyclads.
The Platyhelminthia have most of their organ systems reduced
and simplified; the animals are not therefore primitive. The
coelom is reduced to the ciliated ducts of the reproductive organs.
The Acoela are not the most primitive of the Turbellaria (Fig. 37).
The Aschelminthia include the Nematoda, Rotatoria, Gastro-
tricha, Nematomorpha, Kinorhyncha and Priapulida, some of
which show a spiral pattern of cleavage. It is not clear if the
Aschelminthia are a closely related group of animals.
The Mollusca and Annelida are derived from a common
ancestry. The ventral pharyngeal sac of the archiannelids is
similar to the radula sac of the molluscs and the teeth of the
Eunicidae show plates that are similar to the radula teeth. The
primitive molluscs such as Neopilina may be segmented.
The Articulata (Arthropoda) arose several times from the annelid
stock. The Pentastomida, Onychophora and Tardigrada are three
groups that are quite distinct from one another, though similarities
between the legs, body cavity and gonads can be used to form a
link between the Tardigrada and the Onychophora. The Trilobita
gave rise to the Arachnomorpha. The crustacean resemblances
of the trilobites are due to homoiology; the independent deriva-
tion of similar structures in separate lines that are phylogenetically
related. (Other examples of homoiologous organs are compound
eyes, trachea and malpighian tubules.) The basic line that gave
rise to the Crustacea also gave rise to the Antennata from which
came the Myriapoda and the Insecta.
The Deuterostomia are a smaller and more compact group than
the Protostomia. The hemichordates contain the Enteropneusta
and the Pterobranchiata. The Enchinodermata and the Enter-
opneusta are linked together by the dipleurula larva. The
ancestor of the Hemichordata then being postulated as giving rise
to the Tunicata and the Vertebrata.
Hadzi Classification
The relationship that Hadzi (1944, 1957) postulates between
the various invertebrate groups can be seen from Fig. 38. He
derives the Metazoa from the Ciliophora. In the ciliates there is
THE INVERTEBRATE PHYLA
109
Mommolia
Reptilia-
Amphibia -
Insecta
Apterygogenea
Diplopoda
Chilopoda
Protracheata
Arthroppdq
Arachnoidea
Xiphosura
Pantopoda
Crustacea
Kamptozoa
Nematomorpha
Nematodes
Acanthocephala
Priapuloidea
Sporozoa
Rhizopoda
Flagellata
Fig. 38. Hadzi's classification of the Invertebrate Phyla.
often a differentiation of the cytoplasm in a manner that can be
compared with the ectoderm, mesoderm and endoderm of the
metazoa. Hadzi thinks that such a ciliate gave rise to a form
resembling an acoelous turbellarian and that the Turbellaria are
the most primitive of the Metazoa. The Turbellaria then gave
rise to the Anthozoa, as has been mentioned on p. 95.
The coelom of the metazoa is traced back to the mesohyal
110 THE INVERTEBRATE PHYLA
(mesoderm) of the ciliates; it is not therefore a new formation.
Various cavities such as the nephridial cavity, blood cavity,
secretory cavities, lymph cavities, rhynchocoel and pericardium
are all regarded as being part of the coleomic system. There are
primary cavities, those without an epithelial lining, and secondary
cavities, those with an epithelial lining. The perigastrocoel is a
space lying alongside the gut and it too has become lined with
epithelium. Those animals that have such a perigastrocoel and
which are also unsegmented Hadzi places in his first metazoan
phylum, the Phylum Ameria. Included in the Ameria are the
following groups: Platyhelminthia, Coelenterata, Gastrotricha,
Rotatoria, Kinorhyncha, Mollusca, Priapuloidea, Acanthocephala,
Nematoda, Nematomorpha, Nemertini and Kamptozoa.
The second phylum is the Phylum Polymeria. These animals
are all segmented and the perigastrocoel becomes initially broken
up to form a series of cavities. In some of the higher Polymeria
the cavities become reduced, as in the Hirudinea. Included in
the Polymeria are the following groups : Annelida, Sipunculoidea,
Echiuroidea, Crustacea, Pantapoda, Xiphosura, Arachnida, Chilo-
poda, Diplopoda and Insecta.
The third phylum is the Phylum Oligomeria. These animals
have at some stage of their development adopted a sessile habit
and this has led to a reduction in body segmentation. In the
Oligomeria are placed the Phoronidea, Brachiopoda, Bryozoa,
Chaetognatha, Echinodermata, Pogonophora, Enteropneusta and
Pterobranchiata.
The fourth phylum is the Phylum Chordonia. In this are placed
the Vertebrata and the Tunicata.
Hadzi does not consider that the higher invertebrates can be
satisfactorily classified into Protostomia and Deuterostomia.
Instead he thinks that the line that gave rise to the higher
arthropods also gave rise to the echinoderms.
Marcus's classification and that of Grobben have more in
common than either has to Hadzi's, the greatest difference being
in the position of the platyhelminthes ; Grobben thinks they are
primitive, Marcus thinks they are advanced. The major difficulty
in their classification lies in the placing of phyla other than the
Annelida, Mollusca, Echinodermata and Protochordata. All the
remaining small phyla are difficult to place. It is possible that some
THE INVERTEBRATE PHYLA 111
of them had an independent evolution from the Protozoa. Even
within the major groups such as the Arthropoda difficulties arise ;
it is becoming more certain that the Arthropoda are not a mono-
phyletic phylum of animals but instead are a grade of organisation
and that this grade has been reached independently many times
from some annelid-like stock (Tiegs and Manton 1958).
It would appear that the relationship between the various
invertebrate phyla is a very tenuous one. There are many phyla
that seem to be isolated from each other, and even those phyla
that seem reasonably close to one another, on detailed examination
show differences as important as their similarities. Though it is
useful to consider that the relationships determined by com-
parative anatomy and embryology give proof of a monophyletic
origin of the major phyla, this can only be done by leaving out
much of the available information. Let us now consider the
invertebrate relationships determined by comparative biochemistry
and see if they lead to any more definite conclusions.
CHAPTER 8
BIOCHEMICAL STUDIES OF
PHYLOGENY
The previous discussions concerning the phylogeny of animals
has been concerned with evidence based mainly on morphological
data. Within recent years, however, biochemical studies have
been used to help determine animal relationships and the results
so obtained have aroused considerable interest. Only two such
studies will be considered here: those concerned with the dis-
tribution of phosphagens and those concerned with the distribution
of sterols through the animal kingdom.
Due mainly to the work of the Cambridge biochemists, con-
siderable interest has been focused on the phosphagens present
in the invertebrates and the work has led to the discovery of a
series of new and interesting chemical compounds. It is now
intended to discuss the " phosphagen story " in some detail.
(1) Phosphagens
In many of the textbooks on comparative biochemistry or
physiology such as those of Baldwin (1940) or Prosser (1952) one
will find the following table.
Arginine Creatine
Phylum and Class
phosphate phosphate
Platyhelminthia
+
Annelida
+
Arthropoda
+
Mollusca :
Lamellibranchiata
+
Cephalopoda
+
112
BIOCHEMICAL STUDIES OF PHYLOGENY 113
Echinodermata :
Asteroidea
+
—
Holothuroidea
+
—
Echinoidea
+
+
Protochordata :
Tunicata
+
—
Enteropneusta
+
-f
Cephalochorda
—
+
Vertebrata
—
+
This table indicates that most of the invertebrates have one type
of phosphagen (arginine phosphate) whilst the vertebrates have
another (creatine phosphate). The echinoderms and the proto-
chordates have both types of phosphagen and this makes it seem
likely that they are the group of invertebrates most closely related
to the vertebrates.
Let us now consider the situation in a little more detail.
In 1927 Eggleton and Eggleton showed that one could extract
a labile organic phosphorus-containing compound from vertebrate
muscle. This compound was called phosphagen and later workers
showed that it was in fact creatine phosphate. After isolation crea-
tine phosphate broke down to form creatine and phosphoric acid.
NH.OP(OH).,
/
HN = = C + H20
N— CH2.COOH
CH3
Creatine phosphate.
NH2
HN = C + H3P04
N— CH2.COOH
CH3
Creatine and phosphoric acid.
114
BIOCHEMICAL STUDIES OF PHYLOGENY
Creatine phosphate (CP) was present in many vertebrate muscles,
thus the Eggletons found it in the muscles of Amphioxus, dogfish,
plaice, frog, snake, tortoise, rabbit and guinea-pig. They were
unable to find it in any of the invertebrate muscle they studied
(Aurelia, Lumbricus, Aplysia, Pecten, Holothuria). Meyerhof
(1928) found that there was a phosphagen present in invertebrate
muscles but that it was not creatine phosphate but arginine
phosphate instead. This he found in Sipunculus, Pecten, Holothuria
and Stichopus muscle.
NH.OP(OH)2
NR
HN = C
HN = C
NH
NH
(CH2)3 + H20
(CH2)3 + H3P04
CH.NH2
COOH
Arginine phosphate
CH.NrL
COOH
Arginine and phos-
phoric acid.
Although it is not strictly within the scope of this book it might
be as well to indicate the function of the phosphagens. They act
as an energy reserve for muscle contraction. The phosphagens are
high-energy compounds and they can phosphorylate adenosine
diphosphate (ADP) to form adenosine triphosphate (ATP).
ADP + CP = ATP + C
When a muscle contracts and performs work, at some stage of the
contraction-relaxation cycle it uses up the ATP and converts it
to ADP. This ADP is reconverted to ATP by means of the
phosphagen. At a later stage, glycolysis (the breakdown of glucose
to carbon dioxide and water) brings about the synthesis of more
high-energy compounds and the phosphagen is re-formed. This
reaction CP + ADP = C + ATP is sometimes called the
Lohmann reaction and the reader can find more details in most
BIOCHEMICAL STUDIES OF PHYLOGENY 115
texts on biochemistry (Harper 1959; Baldwin 1957; Fruton and
Simmons 1958).
A thorough survey of the distribution of phosphagens CP and
AP in the animal kingdom was published in 1931 by Needham,
Needham, Baldwin and Yudkin. In some cases they dissected
out the muscle tissue from the lower animals ; in other cases they
used the whole animal, the method used depending upon the
size and availability of the raw material.
It should be remembered in all the discussions of their experi-
mental work that most of the workers were pioneers in the field
and that present-day criticism of techniques is in no way meant to
be disparaging. It is only too easy to look back over a quarter of a
century of research and, being wise after the event, to point out
the various faults and errors. It is inevitable in a scientific subject
that the years will bring great improvements in techniques which
will then indicate that the previously used methods and con-
clusions were not sufficiently justified. There is but one way of
making sure that one's work will never contain any errors and
that is to do no work.
The technique that Needham et al. used for their analysis of the
phosphagen was as follows. They cooled their material and dis-
sected out the required part. This was then weighed, ground up
with trichloracetic acid, left for 10 min in the cold and then
filtered. The filtrate was neutralised with NaOH and then CaCl2
was added to precipitate the inorganic phosphate. This pre-
cipitate of insoluble calcium phosphate was spun down in a
centrifuge and separated from the supernatant fluid. The
precipitate was dissolved in a few drops of concentrated sulphuric
acid and the inorganic phosphate then determined.
The organic phosphate was still in the supernatant solution and
it might contain the two possible phosphagens, creatine phosphate
and arginine phosphate (CP and AP). These were analysed as
follows. If one places CP (or AP) in acid solution, it hydrolyses
to form either creatine (or arginine) and phosphoric acid. If
molybdate ions are present the CP hydrolyses much more rapidly
than does AP. Thus the determination of phosphate after 15 min
hydrolysis gave an indication of the CP value whilst estimation
after 15 hr gave both CP and AP values. The value of AP could
then be determined by subtraction.
9— IOE
116 BIOCHEMICAL STUDIES OF PHYLOGENY
The results from Needham et al.'s experiments are often
summarised as in the table on page 112, but I should like to present
them here in slightly more detail. (See also the table on p. 117.)
(a) Coelenterates
In Anthea rustica 5-07 g of tentacles gave 0-053 mg of total
phosphate of which 0-04 mg was due to inorganic phosphate.
An experiment on 1-05 g of body wall gave a total phosphate of
0-032 mg and an inorganic level of 0-032 mg. A further experi-
ment on 2-71 g of tentacle from Anthea cereus gave total phosphate
of 0-135 mg and an inorganic level of 0-135 mg. The general
conclusion from these experiments was that the level of phos-
phagens in anemones was too low to be detected.
In the ctenophore Pleurobrachia pileus, 33-67 g of total body
gave a total phosphate of 0-12 mg whilst the inorganic phosphate
came to 0-069 mg. This gave 42% organic phosphate which could
be due to phosphagen.
(b) Platyhelminthes
0-4 g of Planaria vitta gave 0-056 mg of total phosphate of
which 0-042 mg was due to inorganic phosphate. This gave a
value of 24% AP. 0-54 g of Polycelis nigra had a total phosphate
value of 0098 mg and an inorganic phosphate value of 0-084 mg.
Hence the value of AP was 14%.
(c) Nemertines
2-1 g of the whole body of Lineus longissimus gave a total
phosphate of 0-987 mg whilst the inorganic phosphate came to
0-47 mg. This gave a value of 52% for AP. A second reading
taking 1-45 g of body gave a total phosphate of 0-299 mg and an
inorganic phosphate of 0-245 mg. The AP value came to 18%.
(d) Annelids
Three annelids were analysed, Nereis, Sabellaria and Spiro-
graphs. Two experiments were carried out on Sabellaria aheolata.
In one case 1-38 g of whole body were taken which gave a total
phosphate of 0-505 mg, 24% of which was due to phosphagen.
In the other case 2-45 g of body gave a value of 0-789 mg of
total phosphate of which 30% was due to phosphagen.
BIOCHEMICAL STUDIES OF PHYLOGENY
117
In Spirogr aphis brevispira 2-83 g of the body gave 0-768 mg
of total phosphate of which 63% was due to phosphagen. Another
estimation from 3-08 g of body gave 0-925 mg of total phosphate
of which 67% was due to phosphagen.
Table 1. Selected from information in Needham, Needham,
Baldwin and Yudkin (1931) showing the amounts of inorganic
and organic phosphorus-containing compounds in various
invertebrates.
PHOS-
WEIGHT
INOR-
PHAGEN
GROUP
ANIMAL
OF
TOTAL P
GANIC
AS % OF
TISSUE
P
TOTAL P
Coelenterata
Anthea rustica
tentacle
5-07
0-053
0-04
?
body wall
1-05
0032
0-032
0
Anthea cereus
tentacle
2-71
0135
0-135
Ctenophora
Pleurobrachia pileus
33-67
0-120
0-069
42-0
Platyhelminthes
Planaria vitta
0-40
0-056
0-042
24-8
Polycelis nigra
0-54
0-098
0-084
14-8
Nemertina
Linens longissimus
2-10
0-978
0-470
52-5
Annelida
Sabellaria alveolata
Spirographis brevis-
1-38
0-505
0-383
24-1
pira
2-83
0-768
0-281
63-5
Nereis diversicolor
3-45
1-359
0-781
50-3
Sipunculoidea
Sipunculus nudus
1-46
0-660
0-195
71-0
Cephalopoda
Sepia officinalis
fin muscle
1-25
0-935
0-79
15-3
mantle
1-19
2-73
2-50
8-3
Octopus vulgaris
1-66
1-77
1-42
12-7
Echinodermata
Cucumaria planci
0-49
0-037
0-037
0-0
Synapta inhoerens
0-90
0-425
0-315
25-9
Strongylocentrotus
lividus
1-63
0-247
0-020
92-0
Asterias glacialis
3-84
0-308
0-072
76-2
Protochordata
Balanoglossus
salmoneus
0-36
0-101
0-057
42-8
Ascidia mentula
7-03
0-05
0-039
22-5
In Nereis diversicolor seven normal animals were taken in which
the phosphagen ranged from 15% to 81% of the total phosphate.
It is of interest that in these measurements the authors found that
118 BIOCHEMICAL STUDIES OF PHYLOGENY
whilst for the other annelids mentioned the phosphagen was
always AP, in Nereis there appeared to be quite a lot of CP in
five out of the seven normal samples. Thus out of the 15-81%
due to total phosphagen the amount due to CP was 5-57%. The
authors considered that these values of CP were due to errors in
their technique and that creatine phosphate was not actually present.
In Sipunculus nudus one measurement was made from 1-46 g
of body wall. This gave a total phosphate level of 0*66 mg of
which 71 % was due to AP.
(e) Cephalopoda
In Sepia officinalis various parts of the animals were analysed
for phosphagen with the following results :
Expt. 1 Expt. 2 Expt. 3
Fin muscle
4%
15%
7%
Mantle
13%
8%
0%
Funnel
6%
10%
0%
Tentacle
12%
5%
0%
In Octopus vulgaris the values from one animal came to, mantle
33%, funnel 27% and tentacle 12% phosphagen. It is of interest
that in both Octopus and Sepia some of the phosphagen was
apparently due to CP. In five out of the nine cases where phos-
phagen was present in Sepia there were traces of CP present, in
one case it being one-third of the total 6% due to phosphagen.
In Octopus in one case out of the three CP was present, it making
up half of the total 12% due to phosphagen.
(f) Echinoderms
Two measurements on the body wall of Cucumaria planci
showed no phosphagens to be present. However, two other
experiments on the phosphagens of the body wall of another
species of holothuriam, Synapta inhoerens, gave values of 5% and
25% of the total phosphate content as being due to phosphagen.
The phosphagen was AP. Nine experiments on the jaw muscles
from the Aristotle's lantern of Strongylocentrotus lividus gave values
from 42%-92% of the total phosphate as being due to phosphagen.
Analysis showed that about one-third or more of this phosphagen
was due to CP.
BIOCHEMICAL STUDIES OF PHYLOGENY 119
In the spines and muscles of Echinocardium cordatum it was not
possible to detect any phosphagens at all.
In the tube feet of the starfish Asterias glacialis there was only
AP present; this made up 76% and 73% of the total phosphate.
(g) Protochordates
In Balanoglossus salmoneus three readings were taken from
different parts of the body. These showed a range in values of
phosphagen of 14%, 16% and 42% of the total phosphate. In
the case where 42% of the phosphate was due to phosphagen it
was shown that 21% was due to CP whilst the other 21% was due
to AP. In the 14% of phosphagen the value was all due to CP
whilst the other case of 16% was all due to AP.
The values given for Ascidia mentula were given as 22% and
12% of the total phosphate being due to phosphagen (AP). But
as the authors pointed out, from 7 g of tissue they obtained only
0-05 mg of total phosphate and 0-039 mg of inorganic phosphate,
hence the results were not very reliable.
On page 289 of their paper, Needham et al. drew up the
following table.
The animal kingdom could be subdivided into animals that had
(1) No arginine phosphate:
Coelenterata Anthea
(2) Only AP:
Coelenterata Pleurobrachia
Platyhelminthia Planaria, Polycelis
Nemertini Lineus
Annelida Sabellaria, Spiro-
graphs, Nereis
Cephalopoda Sepia, Octopus
Echinodermata Synapta, Asterias
Urochorda Ascidia
(3) CPandAP:
Echinodermata Strongylocentrotus
Hemichorda Balanoglossus
(4) CPonly:
Cephalochorda Amphioxus
Craniata Many species
120 BIOCHEMICAL STUDIES OF PHYLOGENY
They concluded, " If any evolutionary significance may be
attached to these findings, it is probable that they support the
Echinoderm-Enteropneust (Balanoglossus) theory of vertebrate
descent rather than any of the other views which from time to
time have been put forward on this question."
In fact the situation was not quite so simple. Thus though the
majority of invertebrates have arginine phosphate and the
vertebrates have creatine phosphate, the authors found creatine
phosphate in the Annelida {Nereis) and in the Mollusca {Sepia) as
well as in the echinodermata {Strongylocentrotus) and Proto-
chordata {Balanoglossus). In Balanoglossus it was present in only
two of the three specimens analysed.
It would seem that there are no very good grounds for con-
cluding from the phosphagen evidence alone that the echinoderms
and the protochordates are more closely related to the vertebrates
than are, say, the Annelida or the Mollusca.
In 1936 Baldwin and Needham repeated some of the determina-
tions of phosphagens in the echinoderms. There were two
problems in which they were interested; the first concerned the
formation of the phosphagen. There should be an enzyme present
in the tissue that would bring about the phosphorylation of the
nitrogenous base and Baldwin and Needham decided to investigate
the properties of this enzyme. Secondly they were not sure about
the nature of the nitrogenous base in the phosphagen. Though
they had felt it might be arginine and/or creatine their tests for
these compounds were not specific tests but general ones. Thus
the Sakaguchi test for arginine (make the solution alkaline with
NaOH; add a little a-naphthol, then add a drop of sodium
hypochlorite solution — a bright red colour develops) is not really
specific for arginine but is given by the radical marked by a ring.
NH2
\
HN=C
/
Fatty acid group *N-CH2.COOH
CH3 Creatine
BIOCHEMICAL STUDIES OF PHYLOGENY 121
It will not react with creatine since creatine has a CH3 group
substituted for the H on the N marked with a *. However, other
compounds such as glycocyamine (this is creatine without the
CH3 group and with an H instead) will give a positive reaction.
NH2
\
HN=C
/
NH.CH2.COOH
Glycocyamine
The creatine was determined by the Jaffe reaction, which again
is not an absolutely specific test for creatine.
The arginine from the phosphagen in the echinoderm muscle
was thus tested by the Sakaguchi test, by seeing if the muscle
extract could synthesise a phosphagen from arginine and phos-
phate, and thirdly by adding arginase and seeing if urea was given
off.
The jaw muscles from Sphaer echinus granulans were shown to
be capable of synthesising AP (26% of the added phosphoric acid
being converted) and CP (12% of the added phosphoric acid
being converted).
Extracts from the longitudinal muscles of Holothuria tubulosa
gave extracts that could synthesise AP from A and P (though it
should be noted that the Russian workers Verbinskaya, Borsuk
and Kreps (1935) found AP and CP in the muscles of the
holothurian Cucumaria frondosa).
Xeedham and Baldwin also quoted work done by P. Baldwin
on the ophiuorid Ophioderma longicauda and the crinoid Antedon
mediterranea. Ophioderma had CP whilst Antedon had AP.
The conclusion the authors drew from their work was that the
ophiuroids and echinoids and possibly the holothurians had AP
and CP and the other echinoderms (asteroids, crinoids) had only
AP.
Let us see to what use this information is put. Hyman (1950)
in her text on the echinoderms states on p. 700, " Further bio-
chemical evidence supporting the close relationship of echinoids
and ophiuroids concerns phosphagens, or phosphorus carriers, of
122 BIOCHEMICAL STUDIES OF PHYLOGENY
great importance in metabolic processes. . . . Crinoids, holo-
thurians and asteroids have arginine as the phosphorus carrier
whereas creatine serves this function in the ophiuroids and the
echinoids (echinoids also have phosphoarginine). Phospho-
creatine is also characteristic of vertebrates ; creatine in organisms
results from the methylation of glycocyamine and only echinoids
and ophiuroids have the enzymes (methylases) necessary for
performing this reaction. The author is of the opinion that the
closer relationship of ophiuroids to echinoids rather than to
asteroids, as usually supposed, is not to be doubted and therefore
the union of asteroids and ophiuroids into one group is not
admissible. Further the arrangement recently adopted by
palaeontologists according to which the asteroids and ophiuroids
derive from a common somasteroid ancestor and hence are to
be united into one class Stellasteroidea must somehow be wrong."
As the reader will have noticed in the analysis of Needham et al.
(1932) of the phosphagens in the annelids, they found some CP
as well as AP present in Nereis. They decided that this was possibly
due to some fault in their technique and that really only the AP
was present.
The problem was reinvestigated by Baldwin and Yudkin in
1949. They used similar techniques to the previous ones; thus
they differentiated between CP and AP by the rate of hydrolysis
in molybdate solution and they also used the Sakaguchi and the
Vosges-Proskauer test for the amino-acids arginine and creatine,
though neither of these tests, as they pointed out, were absolutely
specific.
Twenty-four different species of polychaetes were tested and in
addition they examined Lumbricus, Phascolosoma and Sipunculus.
The polychaetes are listed below.
Amphitrite johnstoni Lepidometria commensalis
Amphitrite ornata Lumbrinereis sp.
Arabella iricolor Maldane urceolata
Arenicola marina Neanthes virens
Branchiomma vesiculosum Nereis cultrifera
Chaetopterus variopedatus Nereis diversicolor
Cirratulus grandis Orbinia ornata
BIOCHEMICAL STUDIES OF PHYLOGENY 123
Cistenides gouldii Pista palmata
Clymenella torquata Sabella pavonia
Diopatra caprea Sabellaria aheolata
Enoplobranchns sanguinea Spirographs brevispira
Glycera dibranchiata Sthenelais leidyi
They found that many of these animals had CP and AP. Thus
Amphitrite, Arenicola, Cirratulus, Clymenella, Enoplobranchus,
Maldane, Nereis cultrifera, Pista, Sabella, Sabellaria and Spiro-
graphis had AP but no CP. In Chaetopterus, Diopatra, Glycera,
Lumbrinereis and Orbinia there was CP but no AP. In Lnmbricus
there was neither CP nor AP. Phascolosoma and Sipunculus had
only AP. The other polychaetes had AP and CP.
The first impression of Baldwin and Yudkin (1948) was that
there was a correlation between the occurrence of AP and the
sedentary habit since Amphitrite, Sabella, Sabellaria and Spiro-
graphs all had AP and were sedentary, but further investigation
(1949) showed that there was no such correlation. Thus even
closely related genera had different phosphagens: Neanthes virens
(which used to be called Nereis virens) had both CP and AP whilst
Nereis diversicolor had only AP.
There was some doubt whether CP was really creatine phosphate
and AP, arginine phosphate. Thus though CP on hydrolysis gave
a positive Vosges-Proskauer test the authors concluded only
provisionally that it was creatine phosphate and designated it as
' CP ' and not CP.
Similarly the arginine phosphate gave a very weak Sakaguchi
reaction and they doubted if 'AP ' was arginine phosphate. They
preferred to refer to it as annelid phosphagen — ' AP.'
The fact that annelids have CP is of importance in deciding
the phylogenetic importance and significance of the phosphagen.
Thus previously it was shown that the invertebrates had AP whilst
the vertebrates, some echinoderms and some protochordates had
CP. We now see that polychaetes (twelve out of the twenty-four
tested) had CP. This means that either the presence of CP is not
a very good phylogenetic indicator or else that the annelids are
more closelv related to the echinoderms and the vertebrates than
they are to, say, the molluscs.
124 BIOCHEMICAL STUDIES OF PHYLOGENY
Baldwin and Yudkin (1949) also carried out some analyses of
the phosphagens in echinoderms and protochordates. They con-
cluded that the hemichordates and the echinoids were unique in
that they both had CP and AP whilst the other echinoderms
(except for ophiuroids) had only AP. These results were presented
in tabular form and indicated that the vertebrates were derived
from the Echinoderm-Protochordate line.
In fact the evidence for the phylogenetic value of phosphagens
is not very good. Out of the three hemichordates studied,
Balanoglossus salmoneus, Saccoglossus kowalezvsky and Saccoglossus
horsti, only the former has AP whilst the others have CP. Rees
(1958) states that in his analysis of twenty specimens of Balano-
glossus clavigerus he was able to find only CP; there was no
indication of AP.
Amongst the echinoids the jaw muscles of Arbacia punctulata
have only AP and no CP whilst Strongylocentrotus lividus and
Echinus esculentus have both CP and AP. Similarly Griffiths,
Morrison and Ennor (1957) showed that though some echinoids
such as Heliocidaris erythrogramma had both CP and AP, others
such as Centrostephanus rodgersi had AP and no CP. These
authors concluded, " The general assumption of Baldwin and
Needham that both AP and CP are found in the echinoids is thus
disproved and the results emphasise the necessity for examining a
number of species within a class before concluding that a particular
phosphagen is characteristic of the class." If one was to take the
possession of the phosphagens as a serious phylogenetic feature
one might conclude that since the ophiuroids have only CP like
the vertebrates that they in fact are the closest of the echinoderms
to the vertebrates.
The phosphagen story took a new turn in the 1950s when
chromatographic analysis was applied to the guanidine com-
pounds. As we have already seen, the previous workers were only
concerned with two guanidines, creatine and arginine, and they
differentiated these on the rate of hydrolysis and various non-
specific tests. French workers at the Laboratory of Comparative
Biochemistry of the College de France (van Thoai, Roche, Robin
and Thiem, 1953) showed that the annelids contained at least two
other phosphagens. They found these by running ascending
BIOCHEMICAL STUDIES OF PHYLOGENY
125
chromatograms of muscle extracts from Arenicola marina and
Nereis dtiersicolor in either pyricline-water or propanol-acetic-
water and developing the chromatograms in a-naphthol hypo-
bromite which gives a coloured spot with guanidines. They
found that in Arenicola there was the compound taurocyamine
phosphate whilst in Nereis there was glycocyamine phosphate.
NH,
NH<
HN = C
NH
NH.CH2.S03H
Taurocyamine
NH.CH2.COOH
Glycocyamine
NH— PO(OH)2
NH— PO(OH),
HN
HN = C
NH.CH2.S03H
Taurocyamine phosphate
NH.CH2.COOH
Glycocyamine
phosphate
The relationship of these compounds to the other phosphagens
was not as obscure as might be supposed on first sight. Thus van
Thoai and Robin (1951) had shown that an enzyme capable of
methylating various compounds had quite a wide distribution in
the invertebrates and that it was quite possible that this might
methylate glycocyamine to form creatine.
It is probable that glycocyamine phosphate (GP) and tauro-
cyamine phosphate (TP) play a similar role in the body to AP
and CP since there are enzymes that can phosphorylate G and T.
Thus Hobson and Rees (1957) showed that specific phosphokinases
were present in various annelids. The unphosphorylated base was
added to the muscle extract, inorganic phosphate and the appro-
priate buffer. This was then incubated at 40 °C for 15 min and
the phosphagens formed isolated and tested. The results are
shown in the following table.
126
BIOCHEMICAL STUDIES OF PHYLOGENY
Table 2
|UM
OF PHOSPHATE FORMED
ANIMALS
TP
GP
AP
CP
Arenicola marina
5-0
1-25
0
0
Nereis diversicolor
0-4
6-5
0
0
Nereis facata
0
5-8
0
20
Hermione hystrix
0
0
0
4-5
Aphrodite acideata
0
0
0
1-25
Myxicola infundibulum
1-5
0
0
0
Nephthys cacea
0
1-7
0
0-7
From Table 2 it can be seen that Arenicola and Myxicola have
TP whilst Nereis diversicolor has GP as its main phosphagen.
Hermione and Aphrodite have CP whilst none of them had AP.
About the same time Roche and Robin (1954) showed the
presence of CP in the sponge Thetia lyncurium and AP in the
sponge Hymeniacidon caruncula. Hymeniacidon also had glyco-
cyamine (but not GP) whilst Thetia had taurocyamine (but no
TP).
Roche et al. (1957) made a thorough survey of the distribution
of arginine and creatine in the animal kingdom, using the methods
of chromatographic separation and semi-specific chemical tests.
The species that they analysed and the results they obtained are
shown below.
Species
Creatine
Arginine
Sphaerechinus granulans
+
+
Martasterias glacialis
+
+
Amphipholis squamata
+
+
Ophiothrix fragilis
+
+
Leptosynapta inhoerens
+
+
Maia squinado
0
+
Apis mellifica
0
+
Bombyx mori
0
+
Sepia officinalis
0
+
Helix pomatia
0
+
Limnaea stagnalis
0
+
Mytilus edulis
0
+
Ostrea edulis
0
+
BIOCHEMICAL STUDIES OF PHYLOGENY 127
Species Creatine Arginine
Arenicola marina
Audouinia tentacidata
Clymene himbricoides
Dasybranchus caducus
Glycera convoluta
Lineus marinus
Lnmbriconereis
Marphysa sanguinea
Nephthys hombergi
Nereis diversicolor
Sabella pavonina
Scolophus armiger
Lumbricas terrestris
Hirudo medicinalis
Phascolosoma elongatum
Sipuncidus nudus
Ascaris himbricoides
Actinia equina
Anemonia sulcata
Calliactis parasitica
Halicho?idria panicea
Hymeniacidon caruncula
Thetia lyncurium
Tetrahymena geleii
The authors conclude that the very wide distribution of
creatine does not allow one to come to any conclusion concerning
its phylogenetic importance and in particular the presence of
creatine in the echinoderms in no way indicates an affinity or
relationship with the vertebrates. This view is supported by
Ennor and Morrison (1958) in their review of the biochemistry of
phosphagens and related guanidines.
What conclusion can be drawn with regard to the distribution
of phosphagens in the animal kingdom? The first conclusion is
that there is certainly no simple cleavage of the animal kingdom
into vertebrates with CP and invertebrates with AP. Instead it is
clear that both CP and AP are found throughout the invertebrates.
The second conclusion is that one cannot base any phylogenetic
+
+
+
+
+
+
+
+
+
+
0
+
+
+
+
+
0
+
0
+
0
+
+
+
0
+
0
+
0
+
+
+
0
-f
0
+
+
+
+
+
+
+
+
+
+
+
0
+
128 BIOCHEMICAL STUDIES OF PHYLOGENY
speculation on the occurrence of CP or AP since related genera
within a class can differ widely in their phosphagens. The third
conclusion is that it is highly probable that other phosphagens in
addition to the recently discovered GP and TP will be found to
play a role in tissue metabolism.
Thus Seaman (1952) has isolated a phosphagen from Tetra-
hymena gelei that does not appear to be any obvious guanidine
derivative, i.e. not arginine, creatine, taurocyamine or glyco-
cyamine. Van Thoai and Robin (1954) isolated another phosphagen
from the muscles of Lumbricus and called it lombricine. Its
structure is shown below. Lombricine has been further analysed
by Beatty et al. (1959), who have shown that it contains a d-
amino-acid, D-serine.
NH2 NH2
C = NH O CH— COOH
I II I
HN— CH2— CH20 P O— CH2
OH
Lombricine
Robin, van Thoai and Pradel (1957) described a new guanidine
derivative in the leech Hirudo medicinalis but have not as yet
published details of its structural formula.
The function of a scientific theory is to help in our understand-
ing of various pieces of information and to suggest further experi-
ments that will test the validity of the theory. The value of a
theory lies in the extent to which it stimulates the development of
such new experiments. The theory concerning the distribution of
phosphagens throughout the animal kingdom as suggested by
Baldwin and Needham has been a very valuable one when judged
in this manner.
It is becoming clear that the initial impetus that Baldwin,
Needham et al. gave to the study of phosphagens has gathered
momentum and a great deal of new information has been gathered
concerning the chemical nature of phosphagens. What is now
required is a very thorough analysis of material from many genera
throughout the whole of the invertebrates for information as to
BIOCHEMICAL STUDIES OF PHYLOGENY 129
the variety of phosphagens. It is certain that many new chemicals
still remain to be discovered and the biochemical variations will
probably be found to be as great as the more obvious morphological
variations.
From the phylogenetic point of view, therefore, the phosphagens
are not a great deal of assistance. The table shown on p. 112
can now be amended as below.
Other
Phylum
AP
CP
guanidines
Protozoa
+
+
Sponges
+
+
+
Coelenterata
+
+
+
Platyhelminthia
+
Nemertina
+
Nematoda
+
Annelida
+
+
+
Arthropoda
+
Mollusca
+
+
Echinodermata
+
+
Protochordata
+
+
Vertebrata
+
The gaps in the table will be filled as more research is done on
this subject.
(2) Sterols
The phosphagens are not the only compounds that have been
used to indicate phylogenetic relationships. Within recent years
certain sterols have been used to elucidate relationships, though the
work is still at a developmental stage. Some applications of the
sterol studies are as follows.
Hyman (1955) in her volume on the echinoderms does not
follow the normal custom and place the asteroids with the
ophiuroids ; instead she places her chapters in the order Holothuria,
Asteroidea, Echinoidea, Ophiuroidea. Her reasons for doing this
are stated on p. 699. In particular she decides that the ophiuroids
and the asteroids should be separated and the ophiuroids placed
withtheechinoidson the basis of larval development, the possession
of an epineural canal in the ophiuroids, and the possible occurrence
130
BIOCHEMICAL STUDIES OF PHYLOGENY
CH3
CH— CH2.CH2R
Cholesterol
Cholestanol
CH3
CH— CH2CH2R
CH3
CH.CH2.CH2.R
CH3
CH.CH=CH.R
Clionasterol
Porifasterol
CH3
CH — CH=CH.R
Stellasterol
Fig. 39. Sterol structure. This figure shows the structure of various
of the sterols mentioned in the text.
R = — CH2.CH(CH3)<, for Cholesterol and Cholestanol.
R = -CH.(CH3).CH"(CH3)2 for the others.
of a vestibule in the ophiuroids. On p. 700 she states, " Finally, in
recent years workers in comparative biochemistry have produced
striking evidence in favour of this community of ancestry " (i.e.
the ophiuroids with the echinoids and not with the asteroids).
" Bergman (1949 and in a letter) finds that all ophiuroids and
echinoids tested have sterols of Type I, namely cholesterol or some
closely related compound, whereas numerous asteroids tested have
Type II sterols that is, stellasterol or related compounds. The
BIOCHEMICAL STUDIES OF PHYLOGENY 131
sterols of the three crinoids thus far tested belong to Type I, al-
though perhaps a new variety, and those of holothurians classify as
Type II. Further biochemical evidence supporting the close re-
lationship of echinoids and ophiuroids concerns phosphagens or
phosphorus carriers, of great importance in metabolic processes."
Bergman (1949) gives the following table showing the various
species of echinoderms studied and the sterols present in each
(see Fig. 39).
Asteroidea Stellasterol Hitodestrol Cholesterol
Asterias rubens *
Asterias forbesi *
Asterias rollestoni *
Asterias scoparius *
Asterias pectinifera *
Echinoidea
Tripneustes esculentus
Centrechinus antillaram
Lytechinus variegatus
Heliocidenis crassidus
Arbacia punctulata
Holothuria
Holothuria princepo *
Cucumaria chronjhelmi *
Ophiuroidea
Ophiopholis aculeata #?
From this table one can see that the asteroids and the holothur-
ians both possess stellasterol whilst the echinoids and possibly the
ophiuroids have cholesterol. This would link the asteroids and the
holothurians on the 0ne hand and the echinoids and ophiuroids
on the other hand, an arrangement which would agree with that
based on larval characteristics.
Perhaps it will pay us to look at the steroid situation in a little
more detail. Bergman (1949) has given an interesting review of the
distribution of lipids in marine invertebrates with special refer-
ence to the sterols. At one time it was thought that cholesterol was
the only sterol present in these bodies but later work showed that
10— IOE
132 BIOCHEMICAL STUDIES OF PHYLOGENY
there were in fact over twenty different sterols, including optical
isomers, present in the invertebrates and that it is quite likely as
research proceeds that still more will be discovered. These
sterols differ in (1) the length of the side chain, (2) the presence or
absence of double bonds in this side chain, (3) the location of
double bonds in the main sterol skeleton.
Up to 1949 the most studied phylum was the Porifera. This was
due to the fact that they were easily obtained in fairly large
quantities. Over fifty different species of sponges have been
analysed by Bergman and his colleagues and they have obtained
some very interesting results. In the first place they have dis-
covered more than ten different sterols in sponges, only two of
which had been known before. Secondly the presence or absence
of these sterols helped in the elucidation of certain systematic
problems.
For some time a sponge from the Biscayne Bay, Florida, had
been given a variety of names. Some collectors had called it
Suberites distortus, others Suberites tuber culosus. Bergman (1949)
studied the sterols present in this sponge and showed that
clionasterol and poriferasterol were present. Now these sterols
were normally not found in the family Suberitidea but instead
were more often found in the Clionidae or the Choanatidea.
Porifer- Neospongo-
sterol
Cholest-
Clionast-
Porifi
anol
erol
aster
Choanitidae
#
#
Suberitidae
#
Clionidae
#
#
Suberites distortus
*
#
#
Suberites was very carefully examined by Laubenfells, who
showed that there were some small microscleres present in the
tissues. These microscleres were diagnostic of the genus
Anthosigmelia, which is in the family Choanitidea. This then would
mean that the sponge was not a Suberitidae but a Choanitidae and
this would agree with the sterol assay.
A more complex case is present in that of Hymeniacidon
heliophila. This sponge has been described both as Hymeniacidon
heliophila and as Stylotella heliophila. The genus Stylotella is
BIOCHEMICAL STUDIES OF PHYLOGENY 133
normally placed in the family Suberitidae, a family containing only
saturated sterols. Bergman has shown that saturated sterols
are present in this sponge and therefore the sterol assay agrees
with its placing amongst the Suberitidae. Unfortunately the range
of sterols of the family Hymeniacidonidae is not yet known but
there is no reason why this sponge should be transferred from the
genus Hymeniacidon to that of Stylotella. Bergman states, " such
a transfer will remain premature until more is known about the
sterol contents of other species of Hymeniacidon and of the closely
related Halichondria " and he makes his position even more clear
in the statement, " It is dangerous and frequently misleading to
base significant conclusions concerning comparative biochemistry
on data derived from but a few representatives of a given phylum.
This point is apparent when the great diversity of sterols in
Porifera is considered."
To return to the echinoderms it will be remembered that so far
only three types of sterol have been described in the literature
for the echinoderms. There is a likelihood that further study of
the echinoderms will show a greater divergence of the sterols
present in this group and that the cleavage shown in the table on
p. 131 will not be so clearly delineated.
CHAPTER 9
VERTEBRATE PALAEONTOLOGY
The most important evidence for the theory of Evolution is that
obtained from the study of palaeontology. Though the study of
other branches of zoology such as Comparative Anatomy or
Embryology might lead one to suspect that animals are all inter-
related, it was the discovery of various fossils and their correct
placing in relative strata and age that provided the main factual
basis for the modern view of Evolution.
It is unfortunate that the earliest rocks to contain fossils, the
Precambrian and Cambrian, already show representatives of all
the major invertebrate phyla. The earliest rocks are mainly
igneous and it is possible that the fossils that they once contained
have since been boiled away, but there is an alternative view that
the invertebrates suddenly and explosively evolved and had little
or no Precambrian history. Though there is some development of
the various invertebrate fossils, especially within the phyla, our
main examples of the evolution of the major groups of animals
come from our study of the vertebrates. If we ask an under-
graduate to give a brief account of the way in which the vertebrate
palaeontology provides evidence for evolution, his answer may go
rather like this.
" It is possible to date the rocks fairly accurately and in general
the oldest rocks are at the bottom and the youngest rocks are on
the top. There are sometimes cases where the rocks have been
turned over so that the layers are sideways on or upside down, but
careful study soon indicates this and allows one to determine
their correct relative positions. If one studies the vertebrate
remains, one finds that there are no vertebrate fossils in the oldest
rocks. The next oldest rocks have some vertebrate fossils; these
are fragments of simple fishes. The next oldest rocks have fish
134
VERTEBRATE PALAEONTOLOGY
135
and amphibian fossils, the next have fish, amphibian and reptile
fossils, whilst the most recent rocks will have fish, amphibian,
reptile and mammal fossils (see Fig. 40)."
"The most important point is that one never finds a mammal
fossil in rocks that are pre-reptilian ; in fact the finding of a single
mammal fossil in such an early stratum would seriously question
the correctness of evolutionary concepts. Such a fossil has never
been found and the evidence now accumulating strongly supports
the view that the fish gave rise to the amphibia, the amphibia to
the reptiles, and the reptiles to the mammals."
Coenozoic
Cretaceous
Jurassic
Triassic
Carboniferous
Devonian
Cambrian
T
Mammals
Reptiles
Amphibia
Fish
No vertebrate fossils
Fig. 40. Diagram to illustrate a simple view of the level of origin of
the various vertebrate fossils. Note that the sequence runs
Fish-Amphibia-Reptilia-Mammals.
This account, though a simple one, contains one serious fault.
The figure shows not the time of origin of the different classes of
the vertebrates but instead the time of dominance of that class. If
we consider the time of origin we get a more complex picture (Fig.
41). Thus instead of having the reptiles, amphibia, bony fish and
elasmobranch fishes all separated from each other by hundreds of
millions of years, they all arose during the course of less than 100
million years. It is of course difficult to decide just when any of
the groups did arise, but some estimate can be made.
The earliest fossil vertebrates, the Agnatha, are found in the
Silurian (fragments are found in the Ordovician). The next group,
the Placoderms, are found in the Upper Silurian. The bony fish
arose in the Devonian as did also the elasmobranches and the
Amphibia. (It is of interest to note here that there is one school
of thought, examplified by Save Soderberg (1934) and Jarvik
136
VERTEBRATE PALAEONTOLOGY
Coenozoic
_
Cretaceous
Jurassic
Triassic
Mammals
1
Carboniferous
Reptiles
■
1
?
Devonian
Fish Ar;phibia ?
i ■
Cambrian
i ?
? No vertebrate fossils
Fig. 4 1 . Diagram to show a more complex view of the level of origin
of the various vertebrate fossils. Note that the precise time of
origin is often not clear and that the jawed fish, amphibia and
reptilia all arose within a comparatively short time of each other.
(1942), that suggests that the modern amphibia are diphyletic,
the anurans coming from one stock of bony fish whilst the
urodeles came from another; the two lines being separate in the
Early Devonian.)
The reptiles arose in the Carboniferous. There are certain
forms such as Seymouria that are of interest in that they have body
characters that are reptilian and head characters that are amphibian.
Seymouria is sometimes thought of as a link between the Amphibia
and reptiles. Unfortunately Seymouria is found in the Permian
whilst the first reptiles arose in the Pennsylvanian, some 20 or so
million years earlier. The situation concerning the origin of the
mammals is not very much more clear, though the mammals
certainly evolved at a later date than the first reptiles. Just how the
major groups of the mammals evolved is not very clear. Thus we
have three distinct mammalian lines, the Monotremes, the
Marsupials and the Placentals, and there is no good evidence that
all three came from the same reptilian stock. It is quite possible
that many of the mammalian-like characters such as warm-
bloodedness, double circulation through the heart, development
of the neopallium, development of hair and secretion by milk
glands, could be homoiologous and that the mammals resemble the
arthropods in that they are not a phylum but a grade of organisa-
tion that has been achieved many times from a basic stock.
There are other points of interest that arise when we consider
the time of origin of these various groups. On embryological
VERTEBRATE PALAEONTOLOGY 137
grounds it had been considered that cartilage was more primitive
than bone. Thus cartilage appeared in the embryo in most cases
before bone did, and the elasmobranch fishes in many ways
appeared simpler than the bony fish. The elasmobranches were
in fact considered to be more primitive than the bony fish and it
was not till more attention was paid to the palaeontological dating
that it become clear that the elasmobranches were more recent
than the Osteichthyes. The Osteichthyes arose in the Early and
Middle Devonian whilst the elasmobranches arose in the Middle-
Late Devonian. Furthermore most of the fossil groups were bony
when first found but there was a tendency to reduce the ossifica-
tion so that the later forms are less bony and more cartilaginous.
The palaeontological evidence thus indicates that bone is more
primitive than cartilage and in this respect conflicts with ideas
that are derived from embryological studies.
The fact that the groups Agnatha, Placoderms, Osteichthyes,
Chrondrichthyes, Amphibia and Reptiles all arose within a
relatively short time of each other (possibly by explosive evolution,
the explosion lasting over 50 million years) means that one has to
be much more accurate in dating the fossils than if it had taken,
say, 300 million years.
There are two main ways of dating rocks: an objective method
of using radioactive data and a subjective method by which one
analyses the relative position of the rocks and their included
fossils and then comes to conclusions concerning the contempor-
aneity and priority of the different strata. Neither of these
methods is completely free from objection, as we shall now see.
Radioactive dating of rocks
There are various methods by which it is possible to use the
ratio of various radioactive materials to determine the absolute
age of rocks. Some of these will briefly be mentioned here.
The first method is the uranium-lead method, or the so-called
radiogenic lead method. Nier (1939) published a review of this
method as applied to various samples and later reviews of the
subject have been written by Knopf (1948), Kulp (1955, 1956) and
Ahrens (1956). There is also the book by Zeuner (1958) which
discusses the various methods of dating material. The common
lead isotope has the atomic weight of 204, However, other
138 VERTEBRATE PALAEONTOLOGY
isotopes of lead occur and these are formed during the breakdown
of uranium and thorium. Thus
TJ238 ^ Pb206
TJ235 ^ Pb207
1^232 y p]^208
The rate of decay of U238— >- Pb206 is constant and can be deter-
mined by experimental observation. It is usually expressed as a
half-life period, i.e. the time taken for x g of uranium to decay
into x/2 g of uranium. Since the half-life period of the three
reactions above are known it is possible to get three checks on the
age of any piece of rock that contains U235, U238 and Th232. In
less than one million years all three reactions come into equilibrium
and the ratio of the values U238/Pb206; U235/Pb207 and Th232/Pb208
should be constant. The ratio of Pb207/Pb206 should also be con-
stant since the ratio of U235/U238 is constant. This means that on
old rocks all three methods should give results of approximately
the same value.
This radiogenic dating has been of the greatest value in deter-
mining the age of the earth. These studies indicate that the
earth is much older than most people had thought and that it is
of the order of 4,500 million years old. But when the radiogenic
methods are applied to more recent rocks, especially those bearing
fossils, two serious handicaps arise. The first is that this method
can of course only be applied to rocks that contain radiogenic
lead; that is, lead derived from uranium or thorium. These rocks
are usually pegmatites, i.e. rocks formed from the residues after
granite has crystallised out from the liquid mass. This implies
that the material at some stage or another has been molten and
that therefore it is unlikely to contain fossils. Secondly there are
considerable differences in the age as determined from the differ-
ent ratio of the isotopes 206/207, 206/238, 207/235 or 208/232.
Thus Kulp (1955) has published a table giving data for forty-five
different samples of material, the lead ratios being determined by
mass spectrometer; and of these only seven are believed to be
accurate to within 5%. Some are very inaccurate, due, it is
believed, to the loss of radon by diffusion from the rocks in the
series U238/Pb206. Another difficulty is due to the amount of
VERTEBRATE PALAEONTOLOGY 139
non-radiogenic lead present in the material. Where this is
high there is a corresponding high error in the estimation. This
can lead to an error of 700 million years in the exceptional case
of the Caribou Mine, Colorado, where the deposit contained as
much as 97% lead. The correct age of the deposit was 25 million
years old.
From the stratigraphic point of view the radiogenic data is a
little disappointing. Thus Kulp (1955) states, " The only
thoroughly satisfactory sample from a stratigraphic point of view
is the Swedish kolm which contains Upper Cambrian fossils."
Unfortunately the isotopic ages obtained by Nier for this sample
do not agree. Thus:
U238/Pb206 gave 380 million years
Tj235/pb>2 07 gave 440 million years
Pb207/Pb206 gave 800 million years
The correct age appears to be 440 million years and it is probable
that the other values are in error due to radon loss.
There are two other locations of fossiliferous rocks that have
also been accurately radiogenically dated. A pitchblende from
Colorado has been dated as 60 million years old. This had been
placed at the beginning of the Eocene. It will be remembered
that the dating of the Eocene was tentatively done by Matthew
(1914) by estimating the time required for the evolution of the
horse. Matthew decided that it took 45 million years, i.e. he
differed by 15 million years from the radiogenic dating.
All these dates are based on pitchblendes which might have
percolated through into the examined strata and they could in
fact have been derived from some other strata than that in which
they have been discovered. Kulp in discussing the uranium
contents of rocks states that the high uranium concentration is
often associated with a carbonaceous deposit and it is conceivable
that the uranium was accumulated by some biochemical process
before the rock systems became molten.
The fact that pegmatites are few and far between makes it
improbable that the uranium method will have extensive use in
dating fossils. It is more likely that some other method will be of
greater use.
140 VERTEBRATE PALAEONTOLOGY
Potassium method
This is one of the most promising new methods for the dating
of rocks. Potassium is one of the most common elements in rock
and its isotope K40 occurs as 0-0119% of the natural element. K40
decays to form Ca40 by beta emission, the decay having a half-life
period of 1-35 X 109 years. This would take us back 1,000
million years. There is a second path of decay open to K40.
It can capture an electron and turn into A40. This latter system
has not yet been fully worked out but it is probable that both
methods will prove of great use in dating rock strata (Ahrens 1956).
A paper by Mayne, Lambert and York (1959) shows that whereas
the previous methods estimated the Upper Cambrian to be 450
million years old, the K method gives a value of 650 million
years. This would mean that these rocks are some 200 million
years older than previously thought, a point of considerable
interest since it indicates the size of the errors to be expected in
estimates based on other methods.
Subjective Methods
We have, then, as yet, no accurate objective clock that will
allow us to determine the absolute age of the majority of the rocks
of the world. Instead we have to go mainly on stratigraphical
data and there too we find several problems.
From a stratigraphical point of view one cannot state the
absolute age of a given piece of rock ; all that one can do is estimate
the relative age of the rock, and where this is based on the thick-
ness of the deposit and the rate of deposition, the results are bound
to be only approximate. If the various levels are complex and
stratified, then it is often possible to determine contemporaneity,
especially when the strata are close together. The situation is
much more complex when one has to decide if rocks in different
parts of the world are contemporaneous. Thus the great Caledonian
Oregony gave rise to a marked separation of the Devonian and
Silurian rocks in North- West Europe, but this separation is not
found in the Appalachian syncline. Similarly the rock strata in
Maryland, U.S.A., show an unbroken series of deposits from the
Late Silurian to Early Devonian without any sign of a boundary.
To what extent can one place the fishes found in England,
Scandinavia, Germany and the United States in their correct
VERTEBRATE PALAEONTOLOGY 141
relative temporal positions? To what extent can one assume that
the climatic conditions in different parts of the world would not
have affected the distribution of animals so that a local change in
climatic conditions lasting some millions of years did not lead to a
migration of specimens into different parts of the world? For
then, if one decided that strata with similar fossils were of similar
age, one could be in serious error. What is the maximum error
that can be allowed in the estimation of the date of any given
series of rocks? All these questions have to be answered before
one can decide that fish A is earlier than fish B in time.
There is another and in this case a minor difficulty. This
concerns the nature and naming of the strata. There is often some
discussion as to whether a given series of rocks should be placed
at the bottom of one level or the top of another. Thus the
Tremadoc has been placed both at the top of the Cambrian and
also at the bottom of the Ordovician. Another problem concerns
the Downtonian; are these Late Silurian or Early Devonian rocks?
This point is only of importance when the fossils are classified as
Late Silurian or Early Devonian instead of Downtonian. It is
indeed a great tribute to the work of the geologists and palaeonto-
logists that so much agreement has been reached concerning the
dating of the various strata. But it is unfortunate that the
difficulties are often glossed over and only the most simple story
presented. When one is dealing with the evolution of the basic
vertebrate types all within a comparatively short time of each
other, the problem of accurate dating becomes one of critical
importance. Many of the conclusions that we have today are only
tentative ones.
We can state with certainty that the earliest bony fragments are
those of Agnathan fish. These are separated by some 300 million
years from the earliest mammalian fragments. But it is much more
difficult to decide just how much earlier the Agnatha were than the
very first Placoderms; or how much earlier the first Osteichthyes
were than the first elasmobranches, or when the first Amphibia
arose relative to the time of origin of the reptiles. We can believe
that one group arose before the other and there is good evidence
that one group of fossils may be commonly found before another,
but when it comes down to giving a precise date, or even a reason-
able estimation of the time of origin of the groups, it is quite
142 VERTEBRATE PALAEONTOLOGY
another matter. Thus we don't know the time or the source of
origin of the vertebrates. We do not know the relationship
between the Agnatha and the Placoderms. We do not know the
ancestry of the Osteichthyes or Chondrichthyes. We do not know
if the Amphibia are monophyletic or diphyletic. We do not know
if the mammals are monophyletic or polyphyletic.
In spite of the ignorance on these basic points certain changes
have been taking place. Thus in older classifications one could
read about a group called " Pisces." This group is no longer
considered a suitable classiflcatory unit and it has been broken
down into the groups Agnatha, Placoderms, Osteichthyes and so
on. In other words the group " Pisces " was a complex grade of
organisation, a grade corresponding to the " fish level of com-
plexity." Further studies may show that the Amphibia, reptiles
and mammals are all grades of organisation and not necessarily
very closely related groups of animals.
Rates of Evolution
Within recent years the study of genera and species in the
various geological strata has been put on a quantitative basis.
Thus if one studies a group of animals and examines the number of
genera present, say, in the Ordovician and then examines how
many of these genera are present in more recent strata one can
make a calculation of the time over which each genus existed and
from this one mav come to certain tentative conclusions about the
J
evolution of the groups as a whole.
This technique, together with various others, has been applied
with considerable success by G. G. Simpson in his books Tempo
and Mode in Evolution (1944) and The Major Features of Evolution
(1953). These works satisfy two desires in the reader: the first
is for an intelligent approach to fossil animals and the realisation
that they once were living animals; the second is for a treatment of
evolution and palaeontology in a mathematical and symbolic
manner.
Simpson takes two groups, the Lamellibranches and the
Carnivores (excluding the Pinnipedia) and for each draws up a
table showing the number of genera present in the Ordovician,
Silurian, Devonian and so on, and also the level at which each
VERTEBRATE PALAEONTOLOGY 143
genus disappeared. From this information it is possible to draw
a curve showing the percentage of Devonian genera that are alive
at more recent times. From these curves one can see that the
lamellibranches differs from the Carnivora in that the mean
survivorship for a lamellibranch genus is some 78 million years
whilst that for the Carnivora is 6J million years. Simpson con-
cludes, " The data undoubtedly exaggerate the difference for
various reasons, but it is safe to say that the carnivores have
evolved, on the average, some ten times as fast as pelecypods
(lamellibranches) " (1944). This does not mean that all lamelli-
branch genera lasted for 78 million years and hence ten times
as long as each carnivore genus; the values referred to are mean
values.
Simpson's views concerning the mean length of genera have
not gone unchallenged. In particular Williams (1957) has made
some interesting objections to the techniques employed by
Simpson. Williams states, " An ever-increasing number of papers
dealing with the development of fossil groups contains a host of
graphical and numerical devices designed to provide a sober tone
of objectivity to the accompanying text. On the whole they appear
to be extremely useful but there is a real danger that the student
will lose sight of the tenuous and arbitrary nature of most of the
data used in the compilation of such charts, for there is always a
tendency to accept numbers as the only worthwhile facts in papers
of this kind."
Williams goes on to point out that a great deal in such calcula-
tions depends on the nature of the systematics of the groups studied
and whether the systematists working on the groups were
" lumpers " or " splitters." The former group as many species
as possible together into one genus, the latter separate each species
into a separate genus! If a lumper has been at work on a group,
there would be few genera and each would exist for a long period
of geological time. There are also comparatively few genera if a
group has not been " monographed " for some time. (There
appears to be a good correlation between the number of mono-
graphs that has been published on a group and the number of
genera described for such a group (Cooper and Williams 1952).)
When the concept of " lumpers and splitters " is applied to the
Brachiopods, a group that includes Lingida which has remained
144 VERTEBRATE PALAEONTOLOGY
unchanged since the Early Cambrian and which Simpson classifies
as a slowly evolving group, it becomes clear that different views
concerning the survivorship of the genera can be obtained by
examining the genera described in 1894, 1929 or 1956; the mean
life of a genus being 64, 56 or 53 million years respectively. This
would still mean little when compared to the 6J million years
of the carnivore genus, i.e. the brachiopods would appear to have
evolved some seven times more slowly.
Williams then points out that the figure for the carnivores is
that of a small group taken over the climax of their evolutionary
history, i.e. when the carnivores show the greatest variation and
formation of new genera. On the other hand the figures for the
lamellibranches and the brachiopods are taken over the whole
range of the animals' geological record and both groups are
found from almost the earliest geological time. Williams therefore
suggests that it is more logical to consider the climax of evolution
of such group as the brachiopods. This would be the 231 genera
of Ordovician times. The average duration of these genera is 16
million years and some have as short a duration as 10 million years.
Thus if the climax of evolution is taken for both the Carnivora and
Brachiopoda, the difference of the mean duration of each genus
changes from one of 6| million years and 53 million years to one of
6J million years and 16 million years. It would be interesting to
have the similar calculations applied to the lamellibranches and,
say, the early reptiles, the latter showing an explosive type of
evolution that took place some time ago, thus allowing the post-
climax period to be analysed. The example just quoted concerning
the rate of evolution of the Brachiopoda shows how careful one
must be in assuming that conclusions are valid unless one makes
a careful consideration and analysis of the data supporting
these conclusions.
The Evolution of the Horse
It would not be fitting in discussing the implications of Evolu-
tion to leave the evolution of the horse out of the discussion. The
evolution of the horse provides one of the keystones in the teach-
ing of evolutionary doctrine, though the actual story depends to a
large extent upon who is telling it and when the story is being
VERTEBRATE PALAEONTOLOGY 145
told. In fact one could easily discuss the evolution of the story of
the evolution of the horse.
It started when Kowalevsky in 1874 working with European
and Asian forms drew up the scheme shown below.
Equus (Pleistocene- Recent)
HI
Hipparion (Pliocene)
t
Anchitherium (Miocene)
t
Palaeotherium (Eocene)
These fossil types showed the trends in the evolution of the
modern horse, i.e. increase in size of the body, reduction in the
number of digits, molarisation of the premolars, etc, even though
in fact later workers showed that Palaeotherium, Anchitherium
and Hipparion were not even on the main line to the evolution of
the horse. In particular, Kowalevsky was handicapped in studying
only Old World horses whilst it has been clearly shown by the
magnificent work of American palaeontologists such as Marsh,
Cope, Leidy, Osborn and Matthew that the major development
of the horse took place in the New World. In 1917 Lull published
a scheme showing the then current concept of the evolution of the
horse (Fig. 42).
Further research showed that the situation was even more
complex than that illustrated by Lull and in 1951 the scheme
shown in Fig. 43 was a more accurate account of the evolution of
the horse ; it will be noted that instead of a simple direct line the
pattern has become more and more branched.
To the interested non-specialist there are several things that are
puzzling in the accounts of the evolution of the horse. In the first
place it is difficult to find a critical account of the basic information.
The accounts given by Piveteau (1958) and by Matthew (1926)
are more concerned with the names of the intermediate forms and
the basic trends of evolution. The account given by Simpson
(1951) is of great interest and very readable but it is written for a
wider audience. It is necessary to go back to the references given
in Matthew (1926) or the papers of Matthew and Stirton (1930),
146
VERTEBRATE PALAEONTOLOGY
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Equus
Hipparion
Pliohippus
Hipparion
Protohippus
Onohippidion
Hippidion
Anchitherium
Merychippus
Hypohippus
Miohippus
Mesohippus
Epihi
Dpus
Orohippus
Hyracotherium = Eohippus
Fig. 42. Evolution of the horse. The scheme shown here is more
complex than that suggested by Kowalevsky. (From Lull 1918.)
and Osborn (1905, 1918) to get any satisfaction concerning the
fossils themselves.
What does the sceptical reader hope to find out? It takes a
great deal of reading to find out for any particular genus just how
complete the various parts of the body are and how much in the
illustrated figures is due to clever reconstruction. The early
papers were always careful to indicate by dotted lines or lack of
shading the precise limits of the reconstructions, but later authors
are not so careful. Secondly it is difficult to find out just how many
specimens of a given genus are available for study. Thus it is
one thing to know that our information on Hyracotherium is
based on, say, 500 specimens, and another if our information is
VERTEBRATE PALAEONTOLOGY
147
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Onohippidium Porahipporion
Equus
Stylohipparion
Neohipparion
Nannippus
Hipparion
Calippus
Magahippus
Archaeohippus
Hypohippus
Anchitherium
Miohippus
Mesohippus
Epihippus
Orohippus
Hyracotherium
II
Fig. 43. Evolution of the horse. The scheme is more complex than
that suggested by Lull. (After Simpson 1951.)
based on five specimens. In the former case we have a very
good idea of the form of the genus and the extent to which its
characters overlap those of related genera (that is, provided that
the 500 specimens are not just isolated cones of teeth!). A cer-
tain amount of information concerning the number of fossil horses
is available. Thus Simpson (1943) quotes the numbers of
specimens of fossil horses in the American Museum of Natural
History as follows : Lower Eocene 397 ; Middle Eocene 54 ; Upper
Eocene 11; Lower Oligocene 30; Middle Oligocene 125; Upper
Oligocene 39. The same author in his account of horses (1951)
has an appendix " where to see fossil horses." He mentions that
there are some fifty-two mounted skeletons of fossil horses in the
11— IOE
148 VERTEBRATE PALAEONTOLOGY
U.S.A. and probably a total of 100 in the world. There are not
any mounted skeletons of Eohippus> Archaeohippus, Megahippus,
Stylohipparion, Nannippus Calippus, Onohippidium or Parahippus,
and none in the United States of Anchitherium or Hipparion.
There are, however, several thousand of horse fragments
collected in the various museums of the world. It is expecting a
great deal to have fully prepared specimens of all the major genera
of fossil horses. But since the horse is such a key example in the
evolutionary doctrine it is important that our knowledge of the
fragments be collected, possibly in the first place as a card index
system and then later published as a catalogue, so that the results
can be made available in synoptic form to all those interested.
A third problem concerns the validity of the various genera and
generic differences. The number of genera described has in-
creased considerably. Thus Kowalevsky in 1874 knew of three;
Lull in 1917 described fifteen; Simpson in 1945 lists twenty-six
genera. To some extent this is due to the discovery and description
of new material but one wonders how valid these genera really
are.
Another problem concerns the dating of these genera. When
Matthew worked out the time taken for the evolution of the horse,
he came to the conclusion it would take some 45 million years.
His calculation was a rough one but it provided a useful guide.
Since then this calculation has been modified by a uranium dating
which places the Eocene back to 60 million years. Over this
60 million years we have had some twenty-six genera and a large
number of species of fossil horse evolving and it would be of the
greatest interest to know the relative positions of these animals
to one another, together with some indication as to the accuracy
of the relative dating. Thus if we could know the parts of, say,
Mesohippus skeleton that have been found in perfect condition,
the number of specimens, fragments and so on of Mesohippus
that are available, the strata from which each of these was derived,
the degree of contemporaneity of the strata plus or minus so
many million years, then we should have no qualms in accepting
the evidence presented to us. At present, however, it is a matter of
faith that the textbook pictures are true, or even that they are the
best representations of the truth that are available to us at the
present time.
VERTEBRATE PALAEONTOLOGY 149
One thing concerning the evolution of the horse has become clear.
The story of the evolution of the horse has become more and
more complex as further material is collected, and instead of a
simple family tree the branches of the tree have increased in size
and complexity till the shape is now more like a bush than a tree.
In some ways it looks as if the pattern of horse evolution might
be even as chaotic as that proposed by Osborn (1937, 1943) for
the evolution of the Proboscidea, where, " in almost no instance
is any known form considered to be a descendant from any other
known form; every subordinate grouping is assumed to have
sprung, quite separately and usually without any known inter-
mediate stage, from hypothetical common ancestors in the Early
Eocene or Late Cretaceous " (Romer 1949). We now know that
the evolution of the horse did not always take a simple path. In
the first place it is not clear that Hyracotherium was the ancestral
horse. Thus Simpson (1945) states, " Matthew has shown and
insisted that Hyracotherium (including Eohippus) is so primitive
that it is not much more definitely equid than tapirid, rhinocerotid,
etc, but it is customary to place it at the root of the equid group."
Similarly it is clear that though in general the horses did
increase in size, certain genera such as Orohippus, Archaeohippus
and Nannippus appear to have been smaller than their ancestors.
Edinger (1948) from her studies of the casts of the skull and the
brains of fossil horses has concluded that the brain surface of the
early fossil horses was perfectly smooth and that the sulci have
developed at a later date. This would indicate that any resem-
blances that have been drawn between the sulci on the brain of
the modern horse and those of other mammals are either due to
convergent evolution or to homoiology.
It is quite likely that further studies will show that the complex-
ity of horse evolution will prove to be as great as that found in the
Proboscidea, Rhinocerotidea or Camelidae.
CHAPTER 10
CONCLUSIONS
What conclusions, then, can one come to concerning the validity
of the various implications of the theory of evolution? If we go
back to our initial assumptions it will be seen that the evidence is
still lacking for most of them.
(1) The first assumption was that non-living things gave rise to
living material. This is still just an assumption. It is conceivable
that living material might have suddenly appeared on this world
in some peculiar manner, say from another planet, but this then
raises the question, " Where did life originate on that planet? "
We could say that life has always existed, but such an explanation
is not a very satisfactory one. Instead, the explanation that non-
living things could have given rise to complex systems having
the properties of living things is generally more acceptable to most
scientists. There is, however, little evidence in favour of
biogenesis and as yet we have no indication that it can be per-
formed. There are many schemes by which biogenesis could have
occurred but these are still suggestive schemes and nothing more.
They may indicate experiments that can be performed, but they
tell us nothing about what actually happened some 1,000 million
years ago. It is therefore a matter of faith on the part of the
biologist that biogenesis did occur and he can choose whatever
method of biogenesis happens to suit him personally; the evidence
for what did happen is not available.
(2) The second assumption was that biogenesis occurred only
once. This again is a matter for belief rather than proof. It is
convenient to believe that all living systems have the same
fundamental chemical processes at work within them, but as
has already been mentioned, only a few representatives from the
wide range of living forms have so far been examined and even
150
CONCLUSIONS 151
these have not been exhaustively analysed. From our limited
experience it is clear that the biochemical systems within proto-
plasm are not uniform, i.e. there is no established biochemical
unity. Thus we are aware that there are systems other than the
Embden-Meyerhof and the tricarboxylic cycles for the systematic
degradation of carbohydrates; a total of six alternative methods
being currently available. High-energy compounds other than
those of phosphorus have been described; the number of vital
amino-acids has gone up from twenty to over seventy; all these
facts indicate that the biochemical systems may be very variable.
The morphological systems in protoplasm, too, show consider-
able variation. It is possible that some aspects of cell structure
such as the mitochondria and the microsomes might have arisen
independently on several distinct occasions. It is also probable
that two or more independent systems have evolved for the
separation of chromosomes during cell division.
It is a convenient assumption that life arose only once and that
all present-day living things are derived from this unique experi-
ence, but because a theory is convenient or simple it does not
mean that it is necessarily correct. If the simplest theory was
always correct we should still be with the four basic elements —
earth, air, fire and water! The simplest explanation is not always
the right one even in biology.
(3) The third assumption was that Viruses, Bacteria, Protozoa
and the higher animals were all interrelated. It seems from the
available evidence that Viruses and Bacteria are complex groups
both of which contain a wide range of morphological and physio-
logical forms. Both groups could have been formed from diverse
sources so that the Viruses and Bacteria would then be an
assembly of forms that contain both primitive and secondarily
simplified units. They would each correspond to a Grade rather
than a Subkingdom or Phylum. We have as yet no definite
evidence about the way in which the Viruses, Bacteria or Protozoa
are interrelated.
(4) The fourth assumption was that the Protozoa gave rise to
the Metazoa. This is an interesting assumption and various
schemes have been proposed to show just how the change could
have taken place. On the other hand equally interesting schemes
have been suggested to show the way in which the Metaphyta
152 CONCLUSIONS
could have given rise to both the Protozoa and the Metazoa.
Here again nothing definite is known. We can believe that
any one of these views is better than any other according to the
relative importance that we accord to the various pieces of
evidence.
(5) The fifth assumption was that the various invertebrate
phyla are interrelated. If biogenesis occurred many times in the
past and the Metazoa developed on several finite occasions then
we might expect to find various isolated groups of invertebrates.
If on the other hand biogenesis was a unique occurrence it should
not be too difficult to show some relationship between all the
various invertebrate phyla.
It should be remembered, for example, that though there are
similarities between the cleavage patterns of the eggs of various
invertebrates these might only reflect the action of physical laws
acting on a restrained fluid system such as we see in the growth of
soap bubbles and not necessarily indicate any fundamental
phylogenetic relationship .
As has already been described, it is difficult to tell which are the
most primitive from amongst the Porifera, Mesozoa, Coelenterata,
Ctenophora or Platyhelminthia and it is not possible to decide
the precise interrelationship of these groups. The higher
invertebrates are equally difficult to relate. Though the concept
of the Protostomia and the Deuterostomia is a useful one, the
basic evidence that separates these two groups is not as clear cut
as might be desired. Furthermore there are various groups such
as the Brachiopoda, Chaetognatha, Ectoprocta and Phoronidea
that have properties that lie between the Protostomia and the
Deuterostomia. It is worth paying serious attention to the con-
cept that the invertebrates are polyphyletic, there being more than
one line coming up to the primitive metazoan condition. It is
extremely likely that the Porifera are on one such side line and it is
conceivable that there could have been others which have since
died away leaving their progeny isolated; in this way one could
explain the position of the nematodes. The number of ways of
achieving a specific form or habit is limited and resemblances
may be due to the course of convergence over the period of many
millions of years. The evidence, then, for the affinities of the
majority of the invertebrates is tenuous and circumstantial; not
CONCLUSIONS 153
the tvpe of evidence that would allow one to form a verdict of
definite relationships.
(6) The sixth assumption, that the invertebrates gave rise to the
vertebrates, has not been discussed in this book. There are several
good reviews on this subject. Thus Neal and Rand (1939) pro-
vide a useful and interesting account of the various views that have
been suggested to explain the relationship between the inverte-
brates and the vertebrates. The vertebrates have been derived
from the annelids, arthropods, nemerteans, hemichordates and the
urochordates. More recently Berrill (1955) has given a detailed
account of the mode of origin of the vertebrates from the urochord-
ates in which the sessile ascidian is considered the basic form.
On the other hand, almost as good a case can be made to show that
the ascidian tadpole is the basic form and that it gave rise to the
sessile ascidian on the one hand and the chordates on the other.
Here again it is a matter of belief which way the evidence happens
to point. As Berrill states, "in a sense this account is science fiction."
(7) We are on somewhat stronger ground with the seventh
assumption that the fish, amphibia, reptiles, birds and mammals
are interrelated. There is the fossil evidence to help us here,
though many of the key transitions are not well documented and
we have as yet to obtain a satisfactory objective method of dating
the fossils. The dating is of the utmost importance, for until we
find a reliable method of dating the fossils we shall not be able to
tell if the first amphibians arose after the first choanichthian or
whether the first reptile arose from the first amphibian. The
evidence that we have at present is insufficient to allow us to
decide the answer to these problems.
One thing that does seem reasonably clear is that many of the
groups such as the Amphibia (Save Soderberg 1934), Reptilia
(Goodrich 1916) and Mammalia appear to be polyphyletic grades
of organisation. Even within the mammals there is the suggestion
that some of the orders might be polyphyletic. Thus Kleinenberg
(1959) has suggested that the Cetacea are diphyletic, the
Odontoceti and the Mysticeti being derived from separate
terrestrial stocks. (Other groups that appear to be polyphyletic
are the Viruses, Bacteria, Protozoa, Arthropoda (Tiegs and
Manton 1958), and it is possible that close study will show that
the Annelida and Protochordata are grades too.)
154 CONCLUSIONS
In effect, much of the evolution of the major groups of animals
has to be taken on trust. There is a certain amount of circum-
stantial evidence but much of it can be argued either way. Where,
then, can we find more definite evidence for evolution? Such
evidence will be found in the study of modern living forms. It
will be remembered that Darwin called his book The Origin of
Species not The Origin of Phyla and it is in the origin and study of
the species that we find the most definite evidence for the evolution
and changing of form. Thus to take a specific example, the
Herring Gull, Larus argentatus, does not interbreed with the
Lesser Black-backed Gull, Larus fuscus, in Western Europe, the
two being separate species. But if we trace L. argentatus across
the northern hemisphere through North America, Eastern Siberia
and Western Siberia we find that in Western Siberia there is a form
of L. argentatus that will interbreed with L. fuscus. We have here
an example of a ring species in which the members at the ends of
the ring will not interbreed whilst those in the middle can. The
separation of what was possibly one species has been going on
for some time (in this case it is suggested since the Ice Age).
We have of course to decide that this is a case of one species
splitting into two and not of two species merging into one, but
this decision is aided by the study of other examples such as those
of small mammals isolated on islands, or the development of
melanic forms in moths. Details of the various types of speciation
can be found in the books by Mayr, Systematics and the Origin
of Species (1942), and Dobzhansky, Genetics and the Origin of
Species (1951).
It might be suggested that if it is possible to show that the
present-day forms are changing and the evolution is occurring
at this level, why can't one extrapolate and say that this in effect
has led to the changes we have seen right from the Viruses to the
Mammals? Of course one can say that the small observable
changes in modern species may be the sort of thing that lead to
all the major changes, but what right have we to make such an
extrapolation? We may feel that this is the answer to the problem,
but is it a satisfactory answer? A blind acceptance of such a view
may in fact be the closing of our eyes to as yet undiscovered factors
which may remain undiscovered for many years if we believe that
the answer has already been found.
CONCLUSIONS 155
It seems at times as if many of our modern writers on evolution
have had their views by some sort of revelation and they base
their opinions on the evolution of life, from the simplest form to
the complex, entirely on the nature of specific and intra-specific
evolution. It is possible that this type of evolution can explain
many of the present-day phenomena, but it is possible and indeed
probable that many as yet unknown systems remain to be dis-
covered and it is premature, not to say arrogant, on our part
if we make any dogmatic assertion as to the mode of evolution
of the major branches of the animal kingdom.
Perhaps it is appropriate here to quote a remark made by
D'Arcy Thompson in his book On Growth and Form. " If a tiny
foraminiferan shell, a Lagena for instance, be found living today,
and a shell indistinguishable from it to the eye be found fossil in
the Chalk or some still more remote geological formation, the
assumption is deemed legitimate that the species has ' survived '
and has handed down its minute specific character or characters
from generation to generation unchanged for untold millions of
years. If the ancient forms be like rather than identical with
the recent, we still assume an unbroken descent, accompanied by
hereditary transmission of common characters and progressive
variations. And if two identical forms be discovered at the
ends of the earth, still (with slight reservation on the score of
possible ' homoplasy ') we build a hypothesis on this fact of
identity, taking it for granted that the two appertain to a common
stock, whose dispersal in space must somehow be accounted for,
its route traced, its epoch determined and its causes discussed or
discovered. In short, the Naturalist admits no exception to the
rule that a natural classification can only be a genealogical one,
nor ever doubts that ' the fact that we are able to classify organ-
isms at all in accordance with the structural characteristics which
they present is due to their being related by descent.' "
What alternative system can we use if we are not to assume
that all animals can be arranged in a genealogical manner? The
alternative is to indicate that there are many gaps and failures
in our present system and that we must realise their existence.
It may be distressing for some readers to discover that so much
in zoology is open to doubt, but this in effect indicates the vast
amount of work that remains to be done. In many courses the
156 CONCLUSIONS
student is obliged to read, assimilate and remember a vast amount
of factual information on the quite false assumption that know-
ledge is the accumulation of facts. There seems so much to be
learnt that the only consolation the student has is that those who
come after him will have even more to learn, for more will be
known. But this is not really so ; much of what we learn today are
only half truths or less and the students of tomorrow will not be
bothered by many of the phlogistons that now torment our brains.
It is in the interpretation and understanding of the factual
information and not the factual information itself that the true
interest lies. Information must precede interpretation, and it is
often difficult to see the factual data in perspective. If one reads
an account of the history of biology such as that presented by
Nordenskiold (1920) or Singer (1950) it sometimes appears that
our predecessors had a much easier task to discover things than we
do today. All that they had to do was realise, say, that oxygen
was necessary for respiration, or that bacteria could cause
septicaemia or that the pancreas was a ductless gland that secreted
insulin. The ideas were simple; they just required the thought
and the experimental evidence ! Let us have no doubt in our minds
that in twenty years or so time, we shall look back on many of
today's problems and make similar observations. Everything will
seem simple and straightforward once it has been explained. Why
then cannot we see some of these solutions now? There are many
partial answers to this question. One is that often an incorrect
idea or fact is accepted and takes the place of the correct one. An
incorrect view can in this way successfully displace the correct
view for many years and it requires very careful analysis and much
experimental data to overthrow an accepted but incorrect theory.
Most students become acquainted with many of the current
concepts in biology whilst still at school and at an age when most
people are, on the whole, uncritical. Then when they come to
study the subject in more detail, they have in their minds several
half truths and misconceptions which tend to prevent them from
coming to a fresh appraisal of the situation. In addition, with a
uniform pattern of education most students tend to have the same
sort of educational background and so in conversation and dis-
cussion they accept common fallacies and agree on matters based
on these fallacies.
CONCLUSIONS 157
It would seem a good principle to encourage the study of
" scientific heresies." There is always the danger that a reader
might be seduced by one of these heresies but the danger is
neither as great nor as serious as the danger of having scientists
brought up in a type of mental strait-jacket or of taking them so
quickly through a subject that they have no time to analyse and
digest the material they have " studied." A careful perusal of the
heresies will also indicate the facts in favour of the currently
accepted doctrines, and if the evidence against a theory is over-
whelming and if there is no other satisfactory theory to take its
place we shall just have to say that we do not yet know the answer.
There is a theory which states that many living animals can be
observed over the course of time to undergo changes so that new
species are formed. This can be called the " Special Theory of
Evolution " and can be demonstrated in certain cases by experi-
ments. On the other hand there is the theory that all the living
forms in the world have arisen from a single source which itself
came from an inorganic form. This theory can be called the
" General Theory of Evolution " and the evidence that supports
it is not sufficiently strong to allow us to consider it as anything
more than a working hypothesis. It is not clear whether the changes
that bring about speciation are of the same nature as those that
brought about the development of new phyla. The answer will
be found by future experimental work and not by dogmatic
assertions that the General Theory of Evolution must be correct
because there is nothing else that will satisfactorily take its place.
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AUTHOR INDEX
Ahrens, L. H. 137, 140
Amano, S. 12
Aristotle, 14
Baker, J. R. 35, 44, 46, 47, 48
Baldwin, E. 112-124, 128
Balfour, F. M. 69
Beatty, I. M. 128
de Beer, G. 46, 79, 93, 96
van Beneden, E. 71
Bergman, W. 130-133
Bernal, J. D. 8
Berrill, N. 153
Borsuk, V. N. 121
Bonner, J. T. 44
Bouillon, J. 56
Boyden, A. 12, 13
Bresslau, E. 99
Bunting, M. 31
Butschli, O. 32
Carlgren, O. 87
Castiaux, P. 56
Caullery, M. 72, 75
Chargaff, I. 20
Chatton, E. 41
Claus, F. W. 66
Cohen, S. 10
Cooper, G. A. 143
Cuenot. L. 101
Darwin, C. 4, 154
Dawydoff, C. 103
Delage, Y. 29, 69
DOBZHANSKY, T. 154
Dodson, E. O. 72
Doflein, F. 33
Dogiel, V. 41
Duboscq, O. 41, 59
Edinger, T. 149
Eggleton, P. and G. P. 113
Ennor, A. H. 124, 127
Faure-Fremiet, E. 43
Fraenkel-Conrat. H. 19
Franz, V. 33, 47
Fruton, J. S. 20, 115
Fry, B. A. 22
Goette, A. 101
Goodrich, E. S. 153
von Graff, L. 99
Grasse, P. P. 12, 24, 25, 29, 33
Gray, J. 15
Grobben, K. 101-106, 110
Grontved, J. 59
Gurwitsch, A. 15
Hadzi, J. 21, 47, 79, 81, 83, 85,
93-99, 108-110
Haeckel, E. 62, 63, 64, 65, 66, 79,
81, 83, 87
Haldane, J. B. S. 8, 17
Hand, C. 87
Hardy, A. C. 48
Harper, H. 115
Heath, H. 96
Hedley, R. D. 65
Herouard, E. 29
Hershey, A. D. 19
Hobson, G. E. 124
Hollaender, A. 15
Hovasse, R. 30
Huxley, T. H. 76-78
Hyman, L. H. 29, 33, 61, 68, 71, 80,
81, 121, 129
Ishii, M. 19
Ivanov, I. V. 83
Jagersten. G. 66, 67, 68, 81, 83
Jarvik, E. 135
Jeans, J. 16
Johnstone, G. 76
169
170
AUTHOR INDEX
Keilin, D. 9
Klebs, G. 29
Knopf, A. 137
Kleinenberg, S. 153
Komai, T. 85, 89
KORNBERG, H. L. 10
Kowalevski, V. O. 145, 148
Krebs, H. 9, 10
Kreps, E. 121
Krumbach, T. 29, 87
KUKENTHAL, W. 29
Kulp, J. L. 137, 138, 139
Lambert, R. St. J. 140
Lang, A. 89, 90, 91
Lankester, E. R. 27, 29, 30, 65, 69
Lea, D. 18
Lederberg, J. 22
Leuchtenberger, C. 12
LlPMANN, F. 12
Lull, R. 145, 148
Lwoff, A. 30
Luria, S. E. 21
Lynen, F. 12
Lyttelton, R. 16
Manton, S. M. 103, 105, 111, 153
Marcus, E. 81, 99, 106-108, 110
Markham, R. 18
Margrath, K. I. 127
Matthew, W. D. 139, 145
Mayne, K. I. 140
Mayr, E. 154
McConnaughey, B. H. 74
Meister, A. 1 1
Meyerhoff, O. 114
Moore, R. C. 80
Morrison, J. F. 124, 127
Moser, F. 81
Murphey, B. F. 137
Neal, H. V. 153
Needham, D. M. 114-119
Needham, J. 15, 114-119, 128
Nier, A. O. 137
Nordenskiold, E. 156
O'Kane, D. J. 23
Oparin, A. I. 8, 14, 16, 17, 23, 25
Osborn, H. F. 146, 149
Ousdal, A. P. 16
Paley, W. 2
Pantin, C. F. A. 81
Peel, J. 22
Picard, J. 85
Pirie, A. 8
PlVETEAU, J. 145
Pocock, M. A. 60
Pradel, L.-A. 124-128
Pringle, J. W. S. 8
Pringsheim, E. G. 29, 30
Prosser, C. L. 112
Radl, E. 5, 66
Ralph, P. M. 87
Rand, H. W. 153
Rasmont, R. 56
Raven, Ch. 106
Rees, K. R. 124
Reich, W. 15
Remane, A. 81, 106
Robin, Y. 124-128
Robinow, C. F. 22
Roche, J. 124-128
Romer, A. S. 149
Save Soderberg, G. 135, 153
Saville Kent, W. 57, 65, 69
SCHRADER, F. 12
SCHOEFFEL, E. 15
Seaman, G. R. 128
Sedcwick, A. 103, 104, 106
Shapley, H. 17
Simmons, S. 20, 115
Simpson, G. G. 142, 144, 145, 146,
147, 149
Singer, C. 14, 156
Smith, J. D. 18
Smith, K. M. 18
Spooner, E. T. C. 22
Stirton, R. A. 145
Stocker, B. A. D. 22
Stunkard, H. 72
Summers, F. M. 43, 48
Swann, M. M. 12
Takahashi, W. N. 19
Thiem, N. 124-126
Thoai, Ng-V. 124-128
Thompson, R. W. 137
Thompson, W. D'Arcy, 155
Tiegs, O. Ill, 153
Tuzet, O. 59, 61
Ulrich, W. 27,44,81, 106
Verbinskaya, N. A. 121
Vendermeerssche, G. 56
Virgil, 14
Wang, Y. L. 9
AUTHOR INDEX
171
Wheeler, L. R. 14
Williams, A. 143, 144
Williams, R. 19
Willmer, E. N. 31, 44, 49
WOHLER, F. 7
York, D. 140
Yudkin, J. 114-119
Yudkin, W. H. 122, 123, 124
Zeuner, F. 137
Zinsser, H. 22
SUBJECT INDEX
Acoela, 83, 95, 98-100
Aequorea, 85
Alcyonium, 79
Algae, relation to Protoza, 33-35
relation to Metazoa, 46-48
Ameria, 94, 110
Amino acids, 11
Amoeba, 26, 35
Amphioxus, 65, 83, 97, 119
Amphipholis, 126
Ammonia, 127
Annelid superphylum, 105
Antedon, 121
Anthea, 116, 117, 119
Anthosigmelia, 132
Anthozoa, 68, 79, 81, 82, 83, 93
Antipathes, 82
Anus, 68, 102-105
Apis, 126
Aphrodite, 126
Arbacia, 12, 124, 131
Archigastrula, 66
Articulata, 108
Arginine phosphate, 112 et seq.
Aschelminthes, 108
Ascidia, 117, 119
Assumptions, 6 et seq., 150 et seq.
Astaciis, 102
Astasia, 29, 30
Asterias, 117, 119, 131
Amelia, 76, 79, 114
Autotrophic bacteria, 22-23, 25
Bacteria, relation to Protozoa, 24-25,
151
Bacteriophage, /aa'ng 18, 19
Balanoglossus, 117, 119, 120, 124
Bilateria, 106-107
Bilateral symmetry, 52-54, 81, 90
Biogenesis, 7, 150-151
Bions, 15
Biogenetic fundamental law, 65
Blastopore formation, 101-105
Blastula, 59, 69, 70, 83, 96
Bombyx, 126
Bodoines, 41
Bonellia, 72
Calliactis, 127
Cambridge, 1
Camelidae, 149
Capitella, 102
Carchesium, 41
Caridina, 102
Cellularisation, 43
Centrostephanus, 124
Ceratium, 40
Chemoautotrophs, 22, 23, 24
Chlamydomonas, 26, 29, 36, 37, 47, 95
Chlorophyll, 31
Choanoflagellata, 57
Choanocytes, 54, 55, 70
Cholesterol, 131
Chonotricha, 27
Chordonia, 110
Christianity, 2, 4
Church, 1, 2, 3
Cleavage, in Ctenophores
radial, 92
spiral, 92
Clymene, 127
172
SUBJECT INDEX
Clytia, 83
Cnidaria, 85-87
Coelenterata, 76; Complex characters,
78-79, 96-97
simple characters, 78
most primitive, 79-82
relation to Ctenophora, 84-87
relation to Porifera, 69-70
aberrant forms, 87, 89
Coelom, 105
Coelomata, 104, 106
Coeloplana, 54, 84, 89, 90-94
Colonies, 36 et seq.
Convoluta, 93, 102
Corallium, 78
Ctenodrilus, 102
Ctenophora, ancestry, 84, 95
coelenterate affinities, 76, 84-87
platyhelminth affinities, 89-94
Ctenoplana, 54, 88, 90-94
Cucumaria, 117, 121, 131
Cunina, 85, 86
Cytula, 62, 63
DNA (deoxyribosenucleic acid), 12,
19
Daphnia, 9
Dendrobaena, 102
Deuterostomia, 102-104
Dictyostelium, 44
Dicyema, 72, 73, 75
Dicyemidae, 72, 74-75
Dimorpha, 31
Dinoclonium, 34, 35
Dinofiagellates, 33, 41
Diplodinium {Entodinium) , 26, 27, 28
Earliest fossils, 134
Echinocardium, 117
Echinoderm, relationships, 52, 124,
129
superphylum, 105
Ectoprocta, 76, 152
Elasmobranchs, 135, 137
Embden-Meyerhof cycle, 9, 10, 151
Enantiazoa, 69
Entodinium {Diplodinium), 26, 27, 28
Equus, 145, 147
Euchlora, 84, 85, 86, 87
Eudorina, 37, 38, 40
Euglena, 29, 30
Euglypha, 65
Euplectella, 56
Evolution, definition, 6-7
Bacteria, 22-25
Brachiopoda, 144
Carnivora, 142-144
horse, 144-149
Lamellibranchs, 142-143
life, 13 et seq.
Mesozoa, 50
Metazoa, 36 et seq., 50 et seq.
Platyhelminthia, 50, 94
Porifera, 54-71
Protozoa, 24-25, 32-35
vertebrates, 134 et seq.
viruses, 21
Foraminifera, 33, 44, 65
Fossils, 134-137, 145-149
Fossil stratification, 137-142
Gastrodes, 85, 87
Gastrula, 65-68, 69, 97
Germ layers, 55, 56, 60, 61, 66-68
General theory of Evolution, 7, 157
Giardia, 46
Glycocyamine, 121, 125
Glycocyamine phosphate, 125-128
Glycera, 123, 127
Gonactinia, 116
Gonium, 36, 38
Grade, 21, 35
Grafizoon, 96
Grantia, 59-61
Gymnodinium, 34, 35, 40
Haemoglobin, 8
Halichondria, 127, 133
Haliclystus, 80
Haliphysema, 62, 63-64, 65
Haplozoon, 41, 72
Heliocidaris, 124, 131
Heterotropic bacteria, 23-25
Hermione, 126
High energy bonds, 11, 12
Hirudo, 127, 128
Hitodestrol, 131
Holothuria, 114, 121, 131
Hormiphora, 89
Horses, evolution of, 144 et seq.
Hydra, 11, 79, 81, 82, 83
Hydroctena, 85, 87, 89
Homoiology, 108, 136
Hydrozoa, 68, 76, 77, 79-83, 87,
94-96
Hyracotherium (Eohippus), 146-149
SUBJECT INDEX
173
Implications, 150 et seq.
Ischnochiton, 103
Inversion, of Grantia, 59-61
of Volvox, 60-61
Invertebrate phyla, 101
Invertebrate phylogeny, 101 et seq.
Lampetia, 89
Lead, 137-139
Leacosolenia, 69
Life, on other planets, 17
origin of, 8 et seq., 13 et seq.
Lineus, 116, 117, 119, 127
Lingula, 143-144
Limnaea, 126
Lohmann reaction, 114
Lombricine, 128
Lucernaria, 80
Lumbriconereis, 127
Lumbricus, 114, 122, 127, 128
Maia, 126
Marphysa, 127
Martasterias, 126
Mastigamoeba, 31, 33
Medusa, 79, 80, 83, 87, 96
Melicerta, 54
Mesozoa, 41, 50, 71-76, 152
resemblances to Trematodes, 74
Meteorites, 16, facing 16, facing 17
Metaphyta, 13, 46, 47
Metazoa, origin of, 25, 36 et seq.,
151-152
most primitive, 50 et seq., 82-84
Mitosis, 12
Miracidium, 72, 74, 76
Monerula, 62, 63
Monocystis, 26, 44
Mouth, 68, 102-105
Mycetozoa, 27
Mytilus, 126
Myxicola, 126
Myxobolus, 43, 45
Muller's larva, 90, 96
Naegleria, 31, 44, 49
Natural selection, vii
Nematocysts, 81
Nematoda, 106, 129
Nemertini, 116, 117, 129
Nephthys, 126, 127
Nereis, 102, 116, 117, 118, 119, 120,
122, 123, 125, 126, 127
Nucleic acids, 20
Nucleoproteins, 8
Obelia, 78
Octopus, 72, 117, 118
Oligomeria, 110
Opalina, 33, 46, 47
Ophioderma, 121
Ophiothrix, 126
Origin of, Bacteria, 22-25
Coelenterates, 76-84
life, 7, 150-151
Metazoa, 36 et seq.
Porifera, 54
Protozoa, 26 et seq.
vertebrates, 120, 124, 134 et seq.
viruses, 18-21
Origin of Phyla, 154
Origin of Species, 4-5, 154
Orgones, 15
Orthonectidae, 72, 74-75
Osteichthyes, 137
Ostrea, 126
Palaeontology, 134 et seq.
Palaeotherium, 145
Palmella stage, 37, 47
Paramecium, 26, 46
Pecten, 114
Pegmatites, 138, 139
Peripatus, 102, 103
Pheopolykrikos, 40, 44
Phoronidea, 107
Phosphagens, Protozoa, 129
Coelenterate, 116
sponges, 129
Platyhelminth, 112, 116
annelid, 112, 116, 122-123
cephalopod, 112
echinoderm, 113, 120-122
protochordate, 113, 123
vertebrate, 113, 122
Phosphorus, 113 et seq.
Physalia, 76, 79
Physemaria, 63, 64
Planaria, 116, 117, 119
Planocera, 102
Planula larva, 69, 70, 83, 87
Plasmodiophora, 46
Plas?nodium, 26, 33
Plasmodroma, 33
Platyhelminthes, 50, 67, 72, 89, 94-96,
99-100, 106-107, 116, 129
174
SUBJECT INDEX
Pleodorina, 37, 40
Pleurobrachia, 76, 84, 86, 89, 116, 117,
119
Podarke, 102
Pogonophora, 56, 83, 106
Polycelis, 116, 117, 119
Polycladida, resemblances to Cteno-
phora, 90-94
Polykrikos, 40
Polymeria, 110
Polyp, 79, 80, 83, 96, 97
Polyphyletic, 13, 152, 153
Pomatoceros, 102
Porifera, 50, 54-71, 82, 132, 152
Porpita, 79
Potassium, 140
Poterion, 56
Primitiveness, 51, 54
Proboscidea, 149
Protanthea, 82
Proterospongia, 57
Protostomia, 102-105
Protozoa, origin, 24-25, 46
colonial forms, 36-44, 47, 57 et seq.
interrelationship, 32-35
most primitive, 26, 47
syncytia, 44-47
Protista, 13
Pterobranchiata, 83
Radial symmetry, 52, 96
Radioactive dating of rocks, 137-140
Rates of evolution, 142-144
Rhinoscerotoidea, 149
Rhizoflagellata, 33
Rhopalura, 72, 75
Rickettsia, 21-22
Sabella, 54, 123, 127
Sabellaria, 116, 117, 119, 123
Saccocirrus, 102
Sacculina, 51
Sakaguchi's test, 120, 121
Salpa, 87
Sappinia, 46
Scolecida, 102
Scyphozoa, 68, 78, 79, 80, 81, 82, 84,
87, 93-96
Sepia, 117, 118, 119, 120, 126
Seymouria, 136
Simplicity, 51
Siphonophora, 76
Sipunculus, 114, 117, 118, 127
Special theory of Evolution, 157
Spaer echinus, 121, 126
Spiral cleavage, 92, 105
Spirochona, 27
Spirographs, 116, 117, 123
Sponges, origin, 57, 71
specialised characters, 55-56
simple characters, 55
Spongiaria, 94
Sporozoa, 26, 43, 44, 45, 53
Stellasterol, 130, 131
Sterols, 129-133
Porifera, 132
Echinodermata, 129, 133
Stichopus, 114
Stronglylocentrotus, 117, 119, 124
Stylotella, 132, 133
Suberites, 132
Sulphur, 12, 23
Symmetry, 52-54, 90, see also Radial
symmetry; Bilateral symmetry
Synapta, 117, 119
Syncytia, 39, 44, 46, 63
Taurocyamine, 125
Taurocyamine phosphate, 125-128
Teredo, 103
Tetrahymena, 127, 128
Tetramitus, 31
Tetraplatia, 87, 89
Tentaculata, 107
Thetia, 126
Thiobacillus , 11, 23
Thorium, 138
Trachylina, 78, 84
Trematodes, 72, 94
Tricarboxylic acid cycle, 9, 10, 11
Trichonympha, 26
Trochosphaera, 54
Turbellaria, 83, 89-94, 108
Tubularia, 76, 77
Uranium, 137-139
Velella, 79
Vermes, 35
Vertebrata, 102, 113, 129, 134 et seq.,
153
Viruses, 18-21, 151
Volvox, 37, 39, 40, 44, 46, 57, 59,
60-61
William of Occam, 9
Zoothamnion, 41, 42, 48
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